Control of two-spotted spider mite, Tetranychus urticae, on strawberry by integrating with cyetpyrafen and Phytoseiulus persimilis

Abstract

The two-spotted spider mite (TSSM, Tetranychus urticae Koch) is a significant agricultural pest, particularly in strawberries. Management of TSSM has traditionally relied on synthetic acaricides, but to mitigate dependency on these chemicals, the control of TSSM on strawberry is often combined with biological control measures and chemical control strategies. The predatory mite, Phytoseiulus persimilis, is a promising biological control agent, preying on all TSSM developmental stages. In this study, we examined the toxicity of six common acaricides on TSSM and P. persimilis, and cyetpyrafen was selected due to its highest relative toxicity value. Then, we examined the compatibility of cyetpyrafen with P. persimilis for TSSM management on strawberries. The results suggested that cyetpyrafen revealed no substantial differences in prey consumption or longevity when compared to the control, though minor effects on the development durations of protonymphs and deutonymphs were noted in the subsequent generation. Additionally, cyetpyrafen's toxicity on key pollinators, such as Apis mellifera and Bombus terrestris, was found to be low. Thus, an integrated strategy combining cyetpyrafen (0.83 mg/L) with P. persimilis (predator–prey ratio of 1:30) was examined under laboratory and field conditions. Laboratory trials demonstrated a reduction in mites per leaf from 32.72 to 14.50 within 3 days, correlating to a 70.23% control efficiency. This efficacy increased to 96.04% by day 9 and was sustained until the experiment concluded on day 27. Field trials similarly showed a reduction in TSSM from 53.93 to 9.63 mites/leaf by day 6, achieving an 83.64% control efficiency, and culminated in a 98.46% reduction by day 10. These findings suggested that an integrated approach utilizing cyetpyrafen in conjunction with P. persimilis can be an effective alternative for TSSM management on strawberry plants.

Introduction

Spider mites, such as the two-spotted spider mite (TSSM), Tetranychus urticae Koch, are one of the most pernicious pests impacting agricultural crops globally (Yin et al. 2022; Pekár and Raspotnig 2022), which feed on plant sap by using their piercing-sucking mouthparts, leading to functional damage in leaves and rendering them more susceptible to pathogens and viruses (Beavers et al. 1972; Bensoussan et al. 2016; De Lillo et al. 2021; Nieberding et al. 2022). TSSM has a wide host range and is notably damaging to greenhouse vegetables and fruits, particularly strawberries (Li and Zhang 2021; Park et al. 2005; Meck et al. 2013; Livinali et al. 2014; Akyazi et al. 2019). In 2016, China was the leading global strawberry producer, with an output of 1,801,865 tons (Wu et al. 2020). However, TSSM jeopardizes the physicochemical and nutritional quality of strawberries, significantly reducing their market value (Livinali et al. 2014). Traditional control methods mainly involve acaricides, but their excessive use has led to TSSM resistance, highlighting the dire need for alternative, eco-friendly control strategies (Desneux et al. 2007; Zhang et al. 2022; Hamdi et al. 2023; Xu et al. 2023; Van Leeuwen et al. 2010).

Biological control measures such as predatory mites and natural acaricides are often effective and eco-friendly (Attia et al. 2013; Iskra et al. 2019; Zélé et al. 2020; Nieberding et al. 2022; Cruz-Miralles et al. 2022). Phytoseiulus persimilis Athias-Henriot is a biological agent for the control of tetranychid mite (Basha et al. 2021), which was introduced into China from Chile in 1975 (Takafuji et al. 1976). Adult mites possess the ability to consume all developmental stages of TSSM, whereas their nymphs predominantly prey on TSSM eggs and nymphs (Takafuji et al. 1976). Although P. persimilis is being successfully utilized to manage TSSM populations in various greenhouse-grown plants, including cucumbers, tomatoes, bedding plants, strawberries, and even citrus orchards (Cakmak et al. 2009; Opit et al. 2009; Gontijo et al. 2012; Argolo et al. 2013; Bilbo et al. 2020), their field application is limited by environmental factors and high costs (Croft and Jung 2001; Jung and Croft 2001; Bilbo and Walgenbach 2020). The control of two-spotted spider mite on strawberry is often combined with P. persimilis and chemical control strategies. Therefore, it is important to identify acaricides that are compatible with P. persimilis to develop an integrated control strategy (Ricupero et al. 2022).

In this study, we examined the toxicity of six commonly used acaricides on TSSM and P. persimilis. A candidate chemical was selected based on relative toxicity value, and then, its toxicity on pollinators, Apis mellifera and Bombus terrestris, and impact on P. persimilis were assessed. We explored an integrated control strategy through laboratory and field efficacy trials to establish a sustainable TSSM management approach for strawberries.

Materials and methods

Mites, pollinators, plants

The colony of TSSM were obtained from Nanjing Agricultural University (Nanjing, China) and was reared in a climatic chamber at the condition of 25 ± 1 °C, 70 ± 5% relative humidity and a photoperiod of 16L:8D on leaves of kidney bean Phaseolus vulgaris L plants (21 day-old). The bean plants were cultivated on plastic pots (15 cm in diameter and 12 cm in height). Symptoms of TSSM attack were observed in bean leaves 7–10 days after the infestation, and then, leaves with mites were collected for use in the experiment. Additionally, the colony of mites used in the field trials was naturally infested on strawberry leaves on farm.

The colony of P. persimilis was acquired from Shandong Lubao Technology Co. Ltd (Jinan, China) and was kept in a climatic chamber as described before. The predatory mites were reared in plastic trays (10 cm in length, 5 cm in width and 5 cm in height) covered with insect-proof net (200 mesh), and were fed with TSSM four times per week with each tray received three bean leaves infested with TSSM.

Apis mellifera and Bombus terrestris, the common pollinators for strawberry, were used in this study. Both colonies were obtained from Shandong Lubao Technology Co. Ltd (Jinan, China) and maintained in plastic box (30 cm in length, 10 cm in width and 20 cm in height) surrounded with carton under control conditions of 30 ± 2 °C with 65 ± 5% relative humidity, fed with sucrose solution (50% w/v) ad libitum and kept in darkness until the experiments were carried out.

Akihime strawberry was used in this experiment. Seedlings of strawberry individually grown in 1-L plastic pots (17 cm in diameter and 20 cm in height) were used in laboratory trials. The potted strawberry plants were kept in a greenhouse at the condition of 25 ± 1 °C, 70 ± 5% relative humidity under natural lighting. Field trials were carried out in a greenhouse at a strawberry farm in Jiyang District (Jinan, Shandong Province, China). The strawberry plants were established on September 5, and the experiments were conducted on November 28 during the flowering phase of strawberries. No acaricides were used in experiment areas.

All mites, pollinators and plants were not exposed to acaricides prior to the experiments.

Acaricides

Six commonly used acaricides were chosen in this study, including cyetpyrafen (30%; Shenyang Sciencreat Chemical Co. Ltd), cyflumetofen (20%; Suzhou FMS Plant Protective Agent Co. Ltd), bifenazate (43%; Modern Mind Agricultural Solutions Co. Ltd), spirodiclofen (24%; Bayer Crop Science Co. Ltd), diafenthiuron (50%; Shanghai Hulian Biological Pharmaceutical Co. Ltd) and etoxazole (11%; Sumitomo Chemical Co. Ltd). The detailed information about the six acaricides was shown in Additional file 1: Table S1.

Toxicity of the six acaricides on TSSM and P. persimilis

The toxicity of acaricides on TSSM and P. persimilis was assessed using the dip method (Luo et al. 2018). The acaricides were diluted to multiple concentrations and tested separately (Table 1). The acaricide solution (40 mL) was poured into a Petri dish (90 mm in diameter and 15 mm in height). Adult females of TSSM were glued backside to glass slides with double-sided sticky tape, keeping their legs free. The glass slides were dipped into the acaricide solution for 5 s. Adult females of P. persimilis were dipped into the solution using a fine-bristle brush for 5 s and kept in acrylic chambers (Su et al. 2019) for observation. TSSMs on glass slides and P. persimilis in acrylic chambers were placed in incubators with the same condition mentioned before, and mortality was assessed 24 h later. Mites in the control group were dipped in distilled water. The mites were considered dead if their feet failed to move upon a light touch. 30 mites with uniform individual size were used for each acaricide concentration, and three replicates were conducted for each treatment and control. The results were considered to be acceptable when mortality in the control group was less than 10%.

Table 1 The gradient concentrations of six acaricides for bioassays (mg/L)

The relative toxicity value was used to evaluate the selectivity of acaricides and calculated using the formula: LC₅₀ of P. persimilis/LC₅₀ of TSSM (Yohzi and Keizi 1973). The results, including LC₅₀ with corresponding 95% confidence limits (CL), regression equation, chi-square (χ2) and correlation coefficient, were calculated using the data processing software, DPS v. 19.05 (Tang et al. 2013).

Toxicity of cyetpyrafen on pollinators

The toxicity of cyetpyrafen on A. mellifera and B. terrestris was assessed by acute oral toxicity bioassay and acute contact toxicity bioassay. In acute oral toxicity bioassay, five gradient concentrations (from 0.5 to 5000 mg a.i./L) of cyetpyrafen solution were prepared by diluting cyetpyrafen stock with sucrose water. Worker bees emerged for 3 days were caged individually in containers (7.5 cm in length, 5 cm in width and 9 cm in height). After deprived food for 4 h, different concentrations of cyetpyrafen suspension diluted in 20 μl sucrose water (50%, v/v) were supplied to bees in 2 mL Eppendorf tubes inserted into plastic cages. After the cyetpyrafen solution was consumed, sufficient sucrose water was supplied to the bees. For acute contact toxicity bioassay, the cyetpyrafen suspension was diluted with distilled water to five gradient concentrations (from 0.005 to 50 g a.i./L). Worker bees emerged for 3 days were anesthetized with carbon dioxide, and 2 μl of cyetpyrafen solution was dropped onto the mid-chest of each bee. When the solution evaporated, the bees were removed to the container and fed sucrose water. For both bioassays, bees in the control group were treated with distilled water. 20 worker bees were used for each concentration and three replicates were conducted respectively. The mortality was recorded 48 h later. The results were evaluated according to the Environmental Safety Assessment Test Criteria for Chemical Pesticides. Part 10: Acute Toxicity Test for Bees, published in China, the pesticide was judged as low toxicity when the LD₅₀ > 11.0 μg a. i./bee (Yuan et al. 2014).

Prey consumption of P. persimilis

Three experimental groups were conducted to assess the prey consumption of P. persimilis. In the cyetpyrafen-treated P. persimilis and cyetpyrafen-treated TSSM (TPTT) group, both P. persimilis and TSSM were treated with cyetpyrafen. In the untreated P. persimilis and cyetpyrafen-treated TSSM (UPTT) group, the TSSM was treated with cyetpyrafen, while P. persimilis was treated with distilled water. In the untreated P. persimilis and untreated TSSM (UPUT) group, both P. persimilis and TSSM were treated with distilled water. For cyetpyrafen-treated P. persimilis or TSSM, cyetpyrafen was sprayed on the body of mites gathered on bean leaves using a sprayer at a concentration of 0.83 mg/L (LC₅₀ for TSSM determined in the 24 h acute toxicity test) with a usage of 5 mL. 30 min after the treatment, the surviving mites were picked and kept in separate chambers for 24 h, and then removed to a new chamber with a P. persimilis/TSSM ratio of 1:20. The number of TSSM ingested by P. persimilis in all three groups was counted and recorded 24 h later. 20 P. persimilis with uniform individual size were used for each treatment, and three replicates were performed. Data were analyzed with one-way ANOVA, followed by separation of means using Student–Newman–Keuls post hoc test (P < 0.05).

Life history traits of P. persimilis

TSSMs kept on kidney bean plants were sprayed with cyetpyrafen at a concentration of 0.83 mg/L with a usage of 5 mL per leaf. After 24 h, newly emerged P. persimilis (F₀) female adults were removed to the acrylic chambers individually, and surviving TSSMs from the treated plants were used to feed F₀ until it died (each F₀ was fed with 10 TSSMs per day). The F₀ was mated with adult males on the second day after emergence, and the eggs (F₁) were collected and reared to adults. F₁ adult females were fed the same way as F₀, and eggs (F₂) were counted and recorded daily until F₁ females died. The longevity of F₀, as well as the egg duration, larva duration, protonymph duration, deutonymph duration, adult duration, preadult, adult preoviposition period (APOP) and total preoviposition period (TPOP) of F_1, were recorded. 20 F₀ females and 50 F₁ females were used in this experiment. For control, adult females of P. persimilis were fed with untreated TSSM. All data for P. persimilis were analyzed based on the two-sex age-stage life table with the TWOSEX-MSChart program (Chi et al. 2013) and data were considered as significantly different if P < 0.05.

Laboratory and field trials

72 potted strawberry plants with 5 or 6 leaves were used in laboratory trials. The plants were divided into 12 groups with 6 in each group. For each group, plants were covered with insect-proof net (59 cm in length, 58 cm in width and 60 cm in height, 200 mesh). 100 adult TSSMs were released into each group evenly on leaves to build the mite population, and the number of mites on each leaf was surveyed 5 days later. The experiments would be carried out when the average number of per leaf over 10 (Strong and Croft 1993). Four treatments were settled including biological, chemical, integrated and untreated groups, with each group containing 3 repetitions. For biological treatment, P. persimilis was released evenly on leaves of plants with a predator–prey ratio of 1:15 (referenced by Gong et al. 2015). For chemical treatment, cyetpyrafen was diluted to obtain a concentration of 60 mg/L (the recommended concentration in the field, Chen et al. 2019) with distilled water using 500 mL and sprayed evenly on the back and top sides of the leaves. For integrated treatment, the concentration of cyetpyrafen was 0.83 mg/L with a usage of 500 mL, and 24 h after the solution was sprayed, P. persimilis were released on leaves with a predator–prey ratio of 1:30 (based on pre-assays results). Plants in untreated group were sprayed with 500 mL distilled water. All treatments were performed only once in this experiment. The surviving TSSM population was sampled by selecting one leaf from each plant (six leaves from each group) and the number of mites was counted using a professional eye loop (10 ×) on days 3, 6, 9, 12, 15, 18, 21, 24 and 27. The results in each group were expressed as an average of the six leaves.

In the field trials, 12 cultivated plots were marked and covered with insect-proof net (3 m in length, 1 m in width and 2.3 m in height, 200 mesh), and were randomly divided into 4 groups with each group containing 3 plots. A distance of 3 m was kept between the plots. The number of TSSM in each plot was counted before the experiments. The same treatment as in the laboratory was conducted, except that the usage of cyetpyrafen was changed to 3 L. The population of TSSM survivors was sampled by selecting five plants in each plot and three leaflets were selected in each plant (45 leaves from each group). The number of mites was counted on days 3, 10, 17, 24, and 30. The results in each group were expressed as an average of the 45 leaves.

The control efficiency (%) in different groups was calculated by the rate of population reduction using the formula of (PT − PC)/(100 − PC) × 100%, where PT represents the population reduction rate of the treated group and PC represents the population reduction rate of the control group (Chen et al. 2022). The control efficiency of TSSM under different treatments in the same day was analyzed with one-way ANOVA. If significant differences were detected among treatments, means were separated using Student–Newman–Keuls as post hoc test (P < 0.05).

Results

Toxicity of six acaricides on TSSM and P. persimilis

To select an effective acaricide, the 24 h acute toxicity of six acaricides was tested. LC₅₀ of the six acaricides for TSSM was 3.53 mg/L (cyflumetofen), 0.83 mg/L (cyetpyrafen), 18.26 mg/L (bifenazate), 582.41 mg/L (diafenthiuron), 5108.31 mg/L (etoxazole) and 4436.07 mg/L (spirodiclofen), while LC₅₀ for P. persimilis was 1676.49 mg/L (cyflumetofen), 2696.81 (cyetpyrafen), 28,034.62 mg/L (bifenazate), 52,540 mg/L (diafenthiuron), 22,424.00 mg/L (etoxazole) and 31,811.78 mg/L (spirodiclofen) (Table 2). The results showed that all the acaricides were significantly more toxic to TSSM than to P. persimilis, indicating that all six acaricides had positive selectivity for pest mites.

Table 2 The 24 h acute toxicity and relative toxicity value of six acaricides to P. persimilis and TSSM

The relative toxicity value of each acaricide was calculated, and the results showed that cyetpyrafen had the maximum relative toxicity value of 3264.91 in the 24 h bioassay (Table 2). Based on the above results, cyetpyrafen was selected for further study.

Toxicity of cyetpyrafen on pollinators

Due to the significant role of bee pollination in strawberry production, the toxicity of cyetpyrafen on A. mellifera and B. terrestris was assessed using acute oral and contact bioassays. No bees were dead after 48 h with the highest dose of 100 µg a.i./bee in both assays. According to the relevant standard in China (Yuan et al. 2014), if no bees died with an acaricide dose of 100 µg a.i./bee, there is no need to test higher concentration, and the acaricide was considered as safe to bees. The results indicated that cyetpyrafen has a low toxicity to both pollinators.

Effect on prey consumption of P. persimilis

The influence of cyetpyrafen on prey consumption of P. persimilis was detected. In TPTT group, the number (4.05) of TSSM consumed by P. persimilis was significantly lower than that in UPUT group (5.45) (P < 0.05) (Fig. 1). In UPTT group, an average of 5.20 TSSM was consumed by P. persimilis, which was similar to that of UPUT group (Fig. 1). The results indicated that the consumption of P. persimilis was unaffected as long as the predator mites were not treated directly with cyetpyrafen.

Fig. 1

Consumption of P. persimilis on TSSM with different treatments. The results were expressed as means ± SD, *P < 0.05. TPTT, treated P. persimilis and treated TSSM. UPTT, untreated P. persimilis and treated TSSM. UPUT, untreated P. persimilis and untreated TSSM

Effects on life history traits of P. persimilis

To assess whether the life history traits of P. persimilis was affected when fed on cyetpyrafen-treated TSSM, we detected the longevity of F₀ and the developmental progression of F₁. The results showed that the average longevity of F₀ was 15.65 days, which was similar to that of control (13.75 days) (Table 3). In F₁, the duration of egg and deutonymph stages were 1.78 days and 1.43 days, respectively, which were both significantly longer than that in the control group (1.64 and 0.97 days, respectively) (P < 0.05), while the protonymph stage was 1.28 days, which was significantly shorter than that in the control group (1.51 days) (P < 0.05) (Table 3). However, there was no difference between the two groups in adult preoviposition period (APOP) (Table 3). In addition, the total preoviposition period (TPOP) of F₁ in the treated group (6.21 days) was significantly longer than that in the control group (5.88 days) (P < 0.05). The average number of eggs produced per day (7.65) and the total number of eggs produced (21.61) were similar to those in the control group (Table 3). The results showed that, when P. persimilis was fed with cyetpyrafen-treated TSSM, no effects were found on other detected parameters other than the development duration on egg and nymph of F₁.

Table 3 Longevity, development time and fertility of P. persimilis fed on cyetpyrafen-treated TSSM

Control efficacy in laboratory and field trials

The control efficacy was assessed in laboratory and field trials. In laboratory trials, the number of TSSM in untreated group increased continuously from 20.44 to 122.11 mites/leaf. The population increased rapidly between day 15 and 18, and till day 21, the population remained stable at a high level (Fig. 2). Typical indicators, such as mature TSSM colonies, faded leaves and development of a silk net, were observed on day 27. In contrast, the TSSM population was suppressed in the other three groups with different control efficacy. The number of TSSMs with chemical treatment decreased rapidly in the first 3 days (from 21.72 to 0.67 mites/leaf), resulting in a control efficiency of 97.95% on day 3 and over 99% thereafter (Fig. 2, Table 4). In the biological treated group, TSSM density increased slightly during the first 3 days (from 29.28 to 33.94 mites/leaf), and then, the density decreased slowly and consistently, resulting in 99.64% control efficiency on day 21 (Fig. 2, Table 4). In the integrated treatment group, the number of TSSMs decreased slower than in the chemical treated group, but apparently faster than that in biological treated group. The number of TSSM decreased from 32.72 to 14.50 mites/leaf in 3 days, resulting in a mite control efficiency of 70.23% (Fig. 2, Table 4). At day 6, the control efficiency of the integrated treatment group reached 87.53%, which was lower than that of the chemical treated group (99.32%) but higher than biological treated group (38.90%), and the control efficiency reached 96.04% on day 9, which was similar to that of the chemical treated group, and the control efficiency remained above 96% until the end of the experiment (Table 4). Overall, chemical treatment with cyetpyrafen was the most rapid method to suppress TSSM, and integrated treatment with cyetpyrafen and P. persimilis was the second rapid method, while biological treatment with the release of P. persimilis required the longest time to achieve the same efficacy.

Fig. 2

TSSM populations on strawberry leaves with different treatments in laboratory experiment. The chemical treated group was sprayed with 500 mL cyetpyrafen solution at concentration of 60 mg/L; the biological treated group was released with P. persimilis with a predator–prey ratio of 1:15; the integrated treated group was sprayed with 500 mL cyetpyrafen solution at concentration of 0.83 mg/L, and P. persimilis was released 24 h later with a predator–prey ratio of 1:30; the control group was sprayed with 500 mL distilled water

Table 4 The TSSM control efficiency with different treatments in laboratory experiment

Similar results were observed in field trials. The number of TSSMs in untreated group increased gradually from day 1 to 19 (from 47.30 to 139.81 mites/leaf, Fig. 3), and the density of TSSM increased slightly thereafter. The number of TSSM in the chemical treated group decreased from 50.32 mites/leaf on day 1 to 0.95 mites/leaf in 3 days, resulting in a control efficiency of 98.23% (Fig. 3, Table 5). In the biological treated group, 19 days were cost to suppress the TSSM density from 58.55 mites/leaf to 5.55 mites/leaf, resulting in 95.73% control efficiency (Fig. 3, Table 5). In the integrated treated group, TSSM density decreased from 53.93 to 9.63 mites/leaf in 6 days, with 83.64% control efficiency, and the density reached a relatively low level on day 10 when density reached 1.08 mites/leaf with 98.46% control efficiency (Fig. 3, Table 5).

Fig. 3

TSSM populations on strawberry leaves with different treatments in field experiment. The chemical treated group was sprayed with 3 L cyetpyrafen solution at concentration of 60 mg/L; the biological treated group was released with P. persimilis with a predator–prey ratio of 1:15; the integrated treated group was sprayed with 3 L cyetpyrafen solution at concentration of 0.83 mg/L, and P. persimilis was released 24 h later with a predator–prey ratio of 1:30; the control group was sprayed with distilled water

Table 5 The TSSM control efficiency with different treatments in field experiment

Discussion

Controlling pests through integrated strategies is gaining popularity recently due to its lower impact during the process (Mateos Fernández et al. 2022; Misango et al. 2022). Several novel approaches have been identified as effective integrated strategies to control TSSM. For example, Hata et al. (2016) suggested that intercropping garlic plants between strawberry rows could reduce mite populations, with the results providing insights for developing alternative control methods using plant extracts. Lime sulfur inhibited oviposition and egg viability of TSSM while favoring predatory mites, suggesting that it could be a potential tool for integrated mite pest management (Ajila et al. 2020). Typically, to effectively control pests and reduce economic and environmental costs, integrated strategies often incorporate both biological and chemical agents (Lacey et al. 2015; Ghidiu et al. 2012), and acceptable achievements have been reported before (Rhodes et al. 2006; Iwassaki et al. 2015; Lin et al. 2021). In the present study, we aimed to develop an integrated strategy with predatory mite and acaricide to control TSSM on strawberries.

P. persimilis is widely recognized as one of the most effective predators and has been extensively used to control TSSM on various plants (Argolo et al. 2013; Bilbo et al. 2020). Therefore, P. persimilis was considered as the primary choice as the biological agent for this study. When selecting a chemical agent for the integrated strategy, the acaricides needed to be highly effective in suppressing the pests without harming the predators (Gentz et al. 2010). Adhering to this principle, the toxicity of six acaricides to TSSM and P. persimilis was detected in our study, and the results were evaluated with relative toxicity. Of the six acaricides, cyetpyrafen was found to be the most harmful to TSSM based on 24 h acute toxicity, while diafenthiuron had the least impact on P. persimilis. Based on the relative toxicity value, cyetpyrafen exhibited the highest value among the six acaricides (Table 2). As a result, cyetpyrafen was chosen as the chemical agent for this study.

The life table is an important tool for studying population ecology (Nika et al. 2021; Leroy et al. 2022), as it provides a clear overview of parameters such as survival rate, development time, longevity and fecundity (Chi et al. 2022a; b). The impact of cyetpyrafen on the life history traits of P. persimilis is a key aspect of the combined strategy. Because less acaricide was used in a combined strategy, predators play an important role in maintaining the pest density at a low level. Therefore, the acaricides selected for the combined strategy should be harmless to predators. In this study, we examined the effect of cyetpyrafen on the life history traits of P. persimilis, and the results indicated that when P. persimilis was fed with cyetpyrafen-treated TSSM, only the development duration of egg and nymph in the first generation were affected, with no impact on other detected parameters (Table 3). This indicated that cyetpyrafen showed negligible influence on the life history traits of P. persimilis. The results provided further support for the application of the combined strategy using cyetpyrafen and P. persimilis.

As biological agent plays an important role in the long-term control of pest mites, more attention should be paid to the compatibility between predators and acaricides (Duso et al. 2020). Additionally, to meet the demand for safe and healthy foods, fruits pollinated by insects have the potential to yield significant economic benefits (Klatt et al. 2013). Therefore, a thorough examination of the risks posed by chemical agents used in integrated strategies for predators and pollinators is essential (Gentz et al. 2010). In a previous study, P. persimilis showed tolerance to many acaricides (Schmidt-Jeffris et al. 2021). Similarly, our study revealed that when fed with cyetpyrafen-treated TSSM, P. persimilis showed no change in consumption (Fig. 1), and only minor effects occurred in the next generation of P. persimilis (Table 3). Furthermore, it was observed that neither A. mellifera nor B. terrestris suffered any mortality when exposed to the highest concentration of cyetpyrafen. These results, therefore, indicated that cyetpyrafen was compatible with P. persimilis and could serve as an environmentally friendly option.

The control efficacy of the integrated strategy was evaluated through laboratory and field experiments in our study, and consistent results were observed. In both experiments, the TSSM population decreased rapidly when controlled with recommend concentration of cyetpyrafen (Figs. 2 and 3), suggesting that chemical control had advantages over other methods to some extent (Van Leeuwen et al. 2015; Zhang et al. 2022; Xu et al. 2023). In contrast, it took more than 20 days in both experiments by releasing P. persimilis to achieve the same level of control efficiency as chemical control methods (Figs. 2 and 3, Tables 4 and 5). These results were consistent with previous studies (Fraulo et al. 2007) and indicated that biological control should be considered as a supplementary method when managing pest mites. In the group using an integrated strategy with cyetpyrafen and P. persimilis, the control efficiency reached that in the cyetpyrafen groups 5 days later in both trials (Tables 4 and 5). However, considering the low concentration of cyetpyrafen and the low predator–prey ratio, these results were acceptable, and a greater control efficacy might be achieved with the optimization of cyetpyrafen concentration and predator–prey ratio. Additionally, the integrated strategy contributed to a reduction in acaricides usage, balancing the food safety and the environmental compatibility. Our findings, as well as assessments in various plants, suggested that integrated strategies for controlling TSSM may present a promising alternative for the future (Lacey et al. 2015; Ghidiu et al. 2012). Further evaluations are needed to refine integrated pest management for strawberries.

In present study, we developed an integrated strategy with cyetpyrafen and P. persimilis to control TSSM on strawberries. The selection of cyetpyrafen as the chemical agent in the integrated strategy was based on relative toxicity value and a thorough safety assessment. The control efficacy of this integrated strategy was assessed through both laboratory and field trials, with results indicating that the integrated strategy with cyetpyrafen and P. persimilis was effective in controlling TSSM on strawberries. These findings could potentially provide an alternative method for managing TSSM infestations in the future.