Skip to main content

Evaluation of two predatory mites and acaricide to suppress Tetranychus urticae (Acari: Tetranychidae) on strawberry

Abstract

Background

The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), is a major pest of strawberry. It was necessary to control this mite pest that can reducing the quality and quantity of the fruits. In this regard, the effect of ZORO acaricide, Neoseiulus californicus (McGregor) and Amblyseius swirskii Athias-Henriot for suppressing the naturally occurring T. urticae populations on three strawberry cultivars were investigated.

Results

The two predatory mites and ZORO treatments significantly suppressed the populations of T. urticae below the control in all tested cultivars. In most cases of the current study, significantly lower numbers of T. urticae were generally observed in ZORO and N. californicus treatments compared to A. swirskii treatment. In all cultivars, the overall mean of reduction percentages of T. urticae populations in N. californicus and ZORO treatments were not statistically different, and all were significantly higher than that in A. swirskii treatment.

Conclusion

The present results suggested that the release of N. californicus and the application of ZORO acaricide could be promising strategies for controlling T. urticae on strawberry, although the release of N. californicus appears to be more competent tactic than ZORO acaricide.

Background

The strawberry (Fragaria × ananassa Duchesne) (Family: Rosaceae) is one of the highest consumed fruits over the last two decades worldwide (Albendin et al. 2015). The ripe fresh strawberry fruits are rich in vitamins and minerals (Khunte et al. 2020). In 2017, Egypt occupied the fourth place among the countries of the world in the production of strawberry (FAO 2019). In recent years, the cultivated area of strawberry has been increasing in Egypt (Abd-Elgawad 2019). The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), is a main pest of several crops and attacks more than 1000 various plant species which includes economically important crops worldwide (van Leeuwen et al. 2010, 2015). However, T. urticae is also a major pest-infested strawberry in many countries such as New Zealand (Butcher et al. 1987), Spain (Garcia-Mari and Gonzalez-Zamora 1999), Argentina (Greco et al. 1999), USA (Dara et al. 2018) and Egypt. In strawberry, the high population of T. urticae can decrease the floral and foliar development and therefore reducing the quality and quantity of the fruits (Rhodes et al. 2006).

In Egypt, the chemical control is still widely used for the management of T. urticae in strawberry crop. The rapid developmental rate of spider mites and their high fecundity allows them to attain destructive population levels very quickly (Sato et al. 2007). In addition, they became resistance to several extensively used acaricides (Gerson and Weintraub 2007). Consequently, the extensive use of pesticides led to the outbreaks of T. urticae during the last few decades (Fraulo et al. 2008). Due to the environmental and health hazards resulted from the chemical pesticides as well as their side effects on the non-target organisms (e.g., soil microorganisms (Scheepmaker and van de Kassteele 2011) and predators (Bergeron and Schmidt-Jeffris 2020)), its use has been regulated firmly (Horikoshi et al. 2017). Take into account the economic significance of strawberry, it is important to search for efficient alternatives for the controlling of T. urticae. In this regard, biological control is one of the most economical and environmentally harmless methods of pest controlling for farmers (Cock et al. 2010). In some agricultural systems, the natural enemies can suppress the spider mite populations below levels of the economic damage (Nyrop et al. 1998). Among many natural enemies, phytoseiids are the most important biocontrol agents of T. urticae (McMurtry and Croft 1997). In different countries, phytoseiid mites are successfully used in the management of T. urticae in protected environments and in an open fields (e.g., Strong and Croft 1995; Gerson et al. 2003; Zhang 2003; Croft et al. 2004). However, phytoseiids are commonly used to control T. urticae in strawberry (Raworth 1990; Easterbrook 1992; Garcia-Mari and Gonzalez-Zamora 1999; Easterbrook et al. 2001; Oliveira et al. 2009).

Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) is a phytoseiid mite that has wide range of diets, e.g., several phytophagous mite species (McMurtry and Croft 1997) and pollen (Pascua et al. 2020). On various crops, N. californicus found to be an effective control agents of T. urticae in different countries (Barber et al. 2003; Elmoghazy et al. 2011). Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae) is also one of the most effective biocontrol agents and is used in over 50 countries worldwide (Calvo et al. 2015). This predatory mite is a polyphagous phytoseiid that can feed on several kinds of prey, such as thrips, whiteflies (Calvo et al. 2011) and T. urticae (Xu and Enkegaard 2010). The aim of the current study was to evaluate the effect of an acaricide (ZORO) and the individual release of two predatory mites (N. californicus and A. swirskii) for suppressing the naturally occurring T. urticae populations on three strawberry cultivars.

Methods

Rearing of mites

The two-spotted spider mite, T. urticae, and the two phytoseiid mites (A. swirskii and N. californicus) were obtained from colonies reared in the Laboratory of Acarology, Pests and Plant Protection Department, National Research Centre, Dokki, Cairo, Egypt.

The colony of T. urticae was reared on kidney bean plants, Phaseolus vulgaris L. The stock colonies of the two phytoseiid mites, N. californicus and A. swirskii, were maintained separately on kidney bean leaves placed on wet cotton pads in large trays. The cotton pad was put in the center of each tray, leaving an empty space provided with water to prevent the phytoseiids from escaping. Infested leaves from T. urticae culture were provided to the phytoseiids cultures as food. The trays were kept in an incubator at 28 ± 2 °C, 70 ± 5% RH. For the mass rearing of these predatory mites, the two phytoseiids were released and reared separately on kidney bean plants infested with T. urticae in greenhouses.

Acaricide used

Abamectin (ZORO 3.6% EC) is the acaricide that was used in the present study at the rate of 100 cm3/100 liter of water.

Experimental design

These experiments were conducted to evaluate the effect of ZORO acaricide and the individual release of two predatory mites for suppressing the naturally occurring T. urticae populations on three strawberry cultivars. The tested cultivars (029, Fortona, and Wanter star) were cultivated during the 2018/2019 season in strawberry field located at Markaz Badr, Beheira Governorate, Egypt. The experimented area of each strawberry cultivar was consists of four equal plots (control and three treatments plots) with three replicates/plot. The size area of each treatment plot was about 84 m2 and the plots were completely separated by plastic sheets. Recommended agricultural process were performed.

All the tested strawberry cultivars were naturally infested with all stages of T. urticae. In the present study, four treatments were assessed and included 1) the releases of N. californicus, 2) the releases of A. swirskii, 3) ZORO acaricide, and 4) the untreated control. On the three cultivars, the two predatory mites were released on November 1, 2018, and December 13, 2018, while for A. swirskii an additional release was carried out on January 31, 2019. However, ZORO acaricide had four applications that carried out on November 1, 2018, December 13, 2018, January 31, 2019 and March 7, 2019. Predatory mites were released on bean leaves with an estimated numbers of each phytoseiid. The two predatory mites were released at predator–prey ratio of 1:7.

Mite sampling

Sampling was initiated from the first of November, the date of first treatment (week 0), and continued for 26 weeks after the first treatment. The leaves samples were collected weekly from the three treatments and control of each cultivar till the end of the study. Each week, 10 leaves per replicate (30 leaves/plot) were collected from 10 randomly selected plants and transferred to the laboratory. The numbers of T. urticae (all stages) on each leaf were counted under a stereomicroscope.

Data analysis

A randomized complete block design was used in the present study. For each cultivar, the efficacy of the three treatments on T. urticae population was estimated by comparing the numbers of T. urticae that recorded in the treated plot with those recorded in the control (untreated) plot in each sampling week. We also calculated the reduction percentages of T. urticae in the treated plots of each cultivar according to Henderson and Tilton equation (Henderson and Tilton 1955). For each cultivar, the overall mean of reduction percentages of mite (during the period from the first sample after treatment to the last sample of the study, the weekly values of reduction percentages of mite were averaged over this period to obtain the overall mean of reduction percentages of mite on each treatment) were also calculated at the end of study. All data were subjected to analysis of variance (ANOVA), F test. For comparing the means, Tukey's multiple range test (P < 0.05) was applied. All statistical analysis were performed by Statistical Package of Social Science (SPSS), version 20.

Results

Natural populations of T. urticae occurred in all strawberry experimental plots. On November 1, the pretreatment samples (week 0) revealed that there were no significant differences in T. urticae natural populations among the four experimental plots of each cultivar (029: F = 0.06; P > 0.05, Fortona: F = 0.01; P > 0.05, Wanter star: F = 0.11; P > 0.05) (Fig. 1). For all cultivars, the first treatment was made on November 1. On all tested cultivars, the three treatments significantly reduced the numbers of T. urticae in treated plots as compared to control plot after one week of treatment (029: F = 217.28; P < 0.01, Fortona: F = 140.11; P < 0.01, Wanter star: F = 69.44; P < 0.01) (Fig. 1). However, the numbers of T. urticae in the untreated plots remained significantly higher than those in treated plots on all weeks following the first treatment (all P’s < 0.01). Generally, from week 1 to week 10, the mean numbers of T. urticae in ZORO and N. californicus plots were significantly less than that in A. swirskii plots. By weeks 12 and 13, the mean numbers of T. urticae in ZORO treatment became significantly higher than those in A. swirskii treatment (all P’s < 0.01). During the two weeks followed the third treatment of ZORO and A. swirskii, the numbers of T. urticae significantly reduced by ZORO treatment compared to A. swirskii treatment (all P’s < 0.01). Again by week 17 and 18, the mean numbers of T. urticae in A. swirskii plots were statistically less than that in ZORO plots (all P’s < 0.01). One week after fourth ZORO treatment, T. urticae numbers in both N. californicus and ZORO treatments were significantly lower than that in A. swirskii treatment (all P’s < 0.01). In the last month of the study, N. californicus treatment led to the highest decreases in T. urticae numbers, followed by A. swirskii and ZORO treatments (Fig. 1).

Fig. 1
figure 1

Mean numbers of Tetranychus urticae on three strawberry cultivars after Tetranychus urticae management treatments. The treatments were: Neoseiulus californicus, Amblyseius swirskii release, ZORO acaricide and untreated control

The reduction percentages of T. urticae populations after the treatments of the two phytoseiids and ZORO acaricide on three strawberry cultivars were presented in Fig. 2. For 029, Fortona and Wanter star cultivars, the first samples after predatory mites releasing (week 1) showed that the reduction percentages of T. urticae were reached to 56.16, 58.19 and 67.55% in N. californicus and 44.37, 42.41 and 44.76% in A. swirskii treatments, respectively. In general, this values were declined in both phytoseiid treatments for the following weeks then increased by week 7 (one week after the second release). In A. swirskii plots, the reduction percentages of T. urticae were fluctuated for the following weeks then increased by week 14 (one week after the third release). On the other hand, the reduction percentages of T. urticae in N. californicus treatment were gradually increased from week 7 until attained their peaks (100% reduction) by week 23, 20 and 21, on the aforementioned cultivars, respectively (Fig. 2).

Fig. 2
figure 2

Reduction percentages of Tetranychus urticae populations on three strawberry cultivars after Tetranychus urticae management treatments. The treatments were: Neoseiulus californicus, Amblyseius swirskii release and ZORO acaricide

One week after the first ZORO application, the reduction percentages of T. urticae were 91.26, 94.47, and 93.92% for 029, Fortona and Wanter star cultivars, respectively (Fig. 2). These values gradually decreased during the following weeks then greatly increased by week 7 (1 week after second application) to record 92.84, 91.76 and 97.39% on the aforementioned cultivars, respectively. Once again, these values gradually decreased until week 13 (date of the third application) then increased for only a week followed by a gradual decrease until week 18 (date of the fourth application). In all cultivars, the reduction percentages of T. urticae in ZORO plots were increased by week 19 followed by a gradual decrease in the next three weeks of study (Fig. 2).

In each cultivars, the statistical analysis indicated that the overall mean of reduction percentages of T. urticae were varied significantly among treatments (all P’s < 0.05). The highest value of the overall mean of reduction percentages of T. urticae populations was recorded in N. californicus, while the lowest was recorded in A. swirskii treatments; without significant difference in these values between N. californicus and ZORO treatments in each cultivars (Fig. 3). In each treatment, although the highest value of the overall mean of reduction percentages of T. urticae was recorded on Wanter star cultivar as compared to the other cultivars, these values were not statistically different among the tested cultivars (all P’s > 0.05) (Fig. 3).

Fig. 3
figure 3

The overall mean of reduction percentages of Tetranychus urticae on strawberry cultivars after Tetranychus urticae management treatments. The treatments were: Neoseiulus californicus, Amblyseius swirskii release and ZORO acaricide

Discussion

The predatory phytoseiid mites are an effective tool for T. urticae management in strawberry crop as indicated by previous studies (Easterbrook et al. 2001; Fitzgerald and Easterbrook 2003; Tuovinen and Lindqvist 2014). In the present study, the two phytoseiids and ZORO treatments suppressed the populations of T. urticae below the control in all cultivars (Fig. 1). Although A. swirskii preyed and developed on T. urticae (Xiao et al. 2012; Farazmand and Amirs-Maafi 2020), our study showed that N. californicus suppressed T. urticae populations quickly and better than A. swirskii; perhaps due to the degrees of phytoseiid specialization with regard to their food. Neoseiulus californicus is known to prefer the tetranychid spider mites that producing heavy webbing as prey (e.g., T. urticae) (McMurtry and Croft 1997), while A. swirskii is a generalist phytoseiid that found to prefer other types of prey such as thrips when compared with T. urticae (Xu and Enkegaard 2010). Our results were also in agreement with the study of van Houten et al. (2007) who confirmed that A. swirskii can decelerate the populations of T. urticae but cannot control T. urticae hot spots because it does not enter the colonies with dense webbing. Elmoghazy et al. (2011) found that N. californicus reduced the populations of T. urticae by 87.22%, while A. swirskii reduced the populations of T. urticae by 57.49% on faba bean which is corroborating with our findings.

In general, it was observed that T. urticae populations that naturally occurred on the tested cultivars were dissimilar among these different cultivars (Fig. 1). This variability in tetranychid mite populations on different plant cultivars may be related to the differentiations in cultivar nutritional value (van de Vrie et al. 1972). However, Fahim et al. (2020) reported variations among the strawberry cultivars in their suitability for the reproduction and development of T. urticae, which may be explain the variations in T. urticae populations on the different tested cultivars in our study.

The pest management programs must be aimed to control the agricultural pests, with considerable success in the terms of environmental safety and long-term economic control. Although a number of studies concluded that Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) found to be able to successfully control T. urticae on strawberry in several countries (Cross 1984; Decou 1994; Cross et al. 1996), other studies have displayed additional advantages of N. californicus over P. persimilis. The reproduction of P. persimilis is depending on the existing of Tetranychus mites as prey. Consequently, this phytoseiid has a tendency to disperse after the number of its prey on a crop is greatly reduced as a result of predation (Cakmak et al. 2005) which only offers short-term pest management (Walzer and Schausberger 1999). On the contrary, N. californicus be able to adapt to variations in its prey populations, which provide a stable pest control over time (Castagnoli et al. 1999; Greco et al. 2005). In spite of that N. californicus prefer tetranychid mites as prey, it can survive on other food sources (e.g., thrips and pollen) if spider mite populations were decreased (Gerson et al. 2003; Pascua et al. 2020). Moreover, N. californicus can survive at low RH (Bakker et al. 1993) and can develop on T. urticae at 15–35 °C (Gotoh et al. 2004). However, the potential of N. californicus as a biocontrol agent that can provide a long-term control of T. urticae on strawberry was mentioned by previous studies (Rhodes et al. 2006; Fraulo et al. 2008).

In all cultivars, the overall mean of reduction percentages of T. urticae populations in N. californicus treatments were ranged between 85.69 and 86.64%. (Fig. 3). This proposed that N. californicus may be a promising biocontrol agent for successful management of T. urticae on strawberry. In the same context, the study of Rhodes and Liburd (2006) on strawberry revealed that N. californicus has a potential to successfully suppress spider mites under the economic thresholds. Our present results are in accordance with previous studies that have demonstrated that N. californicus found to be an efficient suppressor of T. urticae in strawberry crop (Greco et al. 2005; Rhodes et al. 2006; Ahn et al. 2010). On the other hand, Cakmak et al. (2009) found that N. californicus did not decrease Tetranychus cinnabarinus Boisduval population. In our study, N. californicus reduced T. urticae populations below the control after its releases at a predator–prey ratio of 1:7, whereas in Cakmak et al. (2009) study, N. californicus was released at a predator–prey ratio of 1:20; perhaps this is the reason why N. californicus did not reduce T. cinnabarinus numbers. In this context, phytoseiid–spider mite ratios < 1:10 are considered promising in other cropping systems (e.g., Hamlen and Poole 1982; Strong and Croft 1995; Opit et al. 2004).

Compared with N. californicus and ZORO treatments, A. swirskii recorded the lowest overall mean of reduction percentages of T. urticae populations on the tested cultivars (Fig. 3). This suggests that both N. californicus and ZORO may be better in decreasing or controlling T. urticae than A. swirskii on strawberry. Presently, ZORO acaricide was very effective and successfully knocked down T. urticae populations for two weeks after each application. By time, T. urticae populations started to increase, and therefore additional ZORO treatments were required to keep T. urticae numbers low. We suggested that using ZORO acaricide in combination with an efficient phytoseiid, like N. californicus, for the control of T. urticae possibly will be an efficient management strategy on strawberry, although further investigation would be required to prove this possibility.

Based on our results, N. californicus generally decreased the populations of T. urticae to an extent similar to ZORO acaricide in all cultivars. In the same way, Cakmak et al. (2009) indicated that P. persimilis suppressed T. cinnabarinus populations to a level equal to chemical control. In this regard, spider mite is considered a serious pest on the plants treated with commercial chemicals due to its ability to develop a resistance against several widely used acaricides (Kim et al. 2006). Additionally, the extensive use of chemical pesticide can lead to negative impact on the environment and its elements (Kumral et al. 2010). This is contrary to the use of biocontrol agents which might allow permanent reduction of the spider mite populations below damaging levels (Abdallah et al. 2012).

In many agricultural systems, biological control found to be an economically and environmentally good alternative to pesticides (van Lenteren and Bueno 2003). Although ZORO acaricide is effective, the costs of its successive applications in the present study are higher than that of N. californicus; since the acaricide may be less profitable. In strawberry, a one-time treatment of N. californicus costs one-third the costs of chemical applications (Fraulo et al. 2008). Besides, the predatory mites can provide a control for the entire season at a costs approximately equal to one abamectin spray (Waite 2002). However, it is essential to take into consideration the costs of control agents and their effectiveness on the environment when selecting a strategy to control T. urticae. Consequently, the release of N. californicus appear to be more competent tactic than ZORO acaricide to provide an efficient management of T. urticae on strawberry.

Conclusion

In conclusion, both ZORO acaricide and N. californicus are very effective for T. urticae control as compared to A. swirskii. However, the present results suggested that the release of N. californicus appears to be more competent strategy for controlling T. urticae than the chemical control on strawberry.

Availability of data and materials

Not applicable.

References

  • Abdallah AA, El-Saiedy EMA, El-Fatih MM, Shoula ME (2012) Effect of some biological and biochemical control agents against certain squash pests. Arch Phytopathol Plant Prot 45(1):73–82

    Article  CAS  Google Scholar 

  • Abd-Elgawad MMM (2019) Plant-parasitic nematodes of strawberry in Egypt: a review. Bull NRC 43:1–13

    Google Scholar 

  • Ahn JJ, Kim KW, Lee JH (2010) Functional response of Neoseiulus californicus (Acari: Phytoseiidae) to Tetranychus urticae (Acari: Tetranychidae) on strawberry leaves. J Appl Entomol 134:98–104

    Article  Google Scholar 

  • Albendin G, Garcia MDC, Molina JM (2015) Multiple natural enemies do not improve two spotted spider mite and flower western thrips control in strawberry tunnels. Chilean JAR 75(1):63–70

    Google Scholar 

  • Bakker FM, Klein ME, Mesa NC, Braun AR (1993) Saturation deficit tolerance spectra of phytophagous mites and their phytoseiid predators on cassava. Exp Appl Acarol 17:97–113

    Google Scholar 

  • Barber A, Campbell CAM, Crane H, Lilley R, Tregidga E (2003) Biocontrol of two-spotted spider mite Tetranychus urticae on dwarf hops by the phytoseiid mites Phytoseiulus persimilis and Neoseiulus californicus. Biocontrol Sci Technol 13:275–284

    Article  Google Scholar 

  • Bergeron PE, Schmidt-Jeffris RA (2020) Not all predators are equal: miticide non-target effects and differential selectivity. Pest Manag Sci 76:2170–2179

    Article  CAS  PubMed  Google Scholar 

  • Butcher MR, Penman DR, Scott RR (1987) Population dynamics of two-spotted spider mites in multiple year strawberry crops in Canterbury. N Z J Zool 14:509–517

    Article  Google Scholar 

  • Cakmak I, Baspinar H, Madanlar N (2005) Control of the carmine spider mite Tetranychus cinnabarinus Boisduval by the predatory mite Phytoseiulus persimilis (Athias-Henriot) in protected strawberries in Aydin, Tukey. Turk J Agric for 29:259–265

    Google Scholar 

  • Cakmak I, Janssen A, Sabelis MW, Baspinar H (2009) Biological control of an acarine pest by single and multiple natural enemies. Biol Control 50:60–65

    Article  Google Scholar 

  • Calvo FJ, Bolckmans K, Belda JE (2011) Control of Bemisia tabaci and Frankliniella occidentalis in cucumber by Amblyseius swirskii. Biocontrol 56:185–192

    Article  Google Scholar 

  • Calvo FJ, Knapp M, van Houten YM, Hoogerbrugge H, Belda JE (2015) Amblyseius swirskii: What made this predatory mite such a successful biocontrol agent? Exp Appl Acarol 65:419–433

    Article  CAS  PubMed  Google Scholar 

  • Castagnoli M, Liguori M, Simoni S (1999) Effects of two different host plants on biological features of Neoseiulus californicus (McGregor). Int J Acarol 25:145–150

    Article  Google Scholar 

  • Cock MJW, van Lenteren JC, Brodeur J, Barratt BIP, Bigler F, Bolckmans K, Consoli FI, Haas F, Mason PG, Parra JRP (2010) Do new access and benefit sharing procedures under the convention on biological diversity threaten the future of biological control? Biocontrol 55:199–218

    Article  Google Scholar 

  • Croft BA, Pratt DA, Luh HK (2004) Low-density release of Neoseiulus fallacis provide for rapid dispersal and control of Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae) on apple seedlings. Exp Appl Acarol 33:327–339

    Article  CAS  PubMed  Google Scholar 

  • Cross JV (1984) Biological control of two-spotted spider mite (Tetranychus urticae) by Phytoseiulus persimilis on strawberries grown in “walk-in” plastic tunnels, and a simplified method of spider mite population assessment. Plant Pathol 33:417–423

    Article  Google Scholar 

  • Cross JV, Burgess CM, Hanks GR (1996) Integrating insecticide use with biological control of two spotted spider mite (Tetranychus urticae) by Phytoseiulus persimilis on strawberry in the UK, pp 899–906. Brighton Crop Protection Conference—Pests and Diseases, 18–21 November 1996, Brighton, UK

  • Dara SK, Peck D, Murray D (2018) Chemical and non-chemical options for managing twospotted spider mite, western tarnished plant bug and other arthropod pests in strawberries. Insects 9:1–10

    Article  Google Scholar 

  • Decou GC (1994) Biological control of the two-spotted spider mite (Acarina: Tetranychidae) on commercial strawberries in Florida with Phytoseiulus persimilis (Acarina: Phytoseiidae). Fla Entomol 77:33–41

    Article  Google Scholar 

  • Easterbrook MA (1992) The possibilities for control of twospotted spider mite Tetranychus urticae on field-grown strawberries in the UK by predatory mites. Biocontrol Sci Technol 2:235–245

    Article  Google Scholar 

  • Easterbrook MA, Fitzgerald JD, Solomon MG (2001) Biological control of strawberry tarsonemid mite Phytonemus pallidus and two-spotted spider mite Tetranychus urticae on strawberry in the UK using species of Neoseiulus (Amblyseius) (Acari: Phytoseiidae). Exp Appl Acarol 25:25–36

    Article  CAS  PubMed  Google Scholar 

  • Elmoghazy MME, El-Saiedy EMA, Romeih AHM (2011) Integrated control of the two spotted spider mite Tetranychu surticae Koch (Tetranychidae) on faba bean Vicia faba (L.) in an open field at Behaira Governorate, Egypt. Int J Environ Sci Eng. 2:93–100

    Google Scholar 

  • Fahim SF, Momen FM, El-Saiedy ESM (2020) Life table parameters of Tetranychus urticae (Trombidiformes: Tetranychidae) on four strawberry cultivars. Persian J Acarol 9(1):43–56

    Google Scholar 

  • FAO. Countries by commodity. 2019; Available at: http://www.fao.org/faostat/en/#rankings/countries_by_commodity (Accessed 10 Mar 2019)

  • Farazmand A, Amir-Maafi M (2020) Oviposition model of Amblyseius swirskii Athias-Henriot in prey system (Tetranychus urticae Koch). Syst Appl Acarol 25(10):1857–1866

    Google Scholar 

  • Fitzgerald J, Easterbrook M (2003) Phytoseiids for control of spider mite, Tetranychus urticae, and tarsonemid mite, Phytonemus pallidus, on strawberry in UK. Bull OILB/SROP 26(2):107–111

    Google Scholar 

  • Fraulo AB, McSorley R, Liburd OE (2008) Effect of the biological control agent Neoseiulus californicus (Acari: Phytoseiidae) on arthropod community structure in North Florida strawberry fields. Flor Entomol 91(3):436–445

    Article  Google Scholar 

  • Garcia-Mari F, Gonzalez-Zamora JE (1999) Biological control of Tetranychus urticae (Acari: Tetranychidae) with naturally occurring predators in strawberry plantings in Valencia, Spain. Exp Appl Acarol 23:487–495

    Article  Google Scholar 

  • Gerson U, Weintraub PG (2007) Mites control for the pests in protected cultivation. Pest Manag Sci 63:658–676

    Article  CAS  PubMed  Google Scholar 

  • Gerson U, Smiley RL, Ochoa R (2003) Mites (Acari) for pest control. Blackwell, Oxford, p 539

    Book  Google Scholar 

  • Gotoh T, Yamaguchi K, Mori K (2004) Effect of temperature on life history of the predatory mite Amblyseius (Neoseiulus) californicus (Acari: Phytoseiidae). Exp Appl Acarol 32:15–30

    Article  PubMed  Google Scholar 

  • Greco NM, Liljesthom GG, Sanchez NE (1999) Spatial distribution and coincidence of Neoseiulus californicus and Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae) on strawberry. Exp Appl Acarol 23:567–580

    Article  Google Scholar 

  • Greco NM, Sanchez NE, Liljesthrom GG (2005) Neoseiulus californicus (Acari: Phytoseiidae) as a potential control agent of Tetranychus urticae (Acari: Tetranychidae): effect of pest/predator ratio on pest abundance on strawberry. Exp Appl Acarol 37:57–66

    Article  CAS  PubMed  Google Scholar 

  • Hamlen RA, Poole RT. Integrated pest management on spider mites. Southern Florist and Nurseryman. January Issue; 1982

  • Henderson CF, Tilton EW (1955) Tests with acaricides against the brow wheat mite. J Econ Entomol 48:157–161

    Article  CAS  Google Scholar 

  • Horikoshi R, Goto K, Mitomi M, Oyama K, Sunazuka T, Omura S (2017) Identification of pyripyropene A as a promising insecticidal compound in a microbial metabolite screening. J Antibiot 70:1–5

    Article  CAS  Google Scholar 

  • Khunte SD, Kumar A, Ansari N, Saravanan S (2020) Effect of different levels of PGRs with organic manure on growth characters and economics of strawberry (Fragaria x ananassa Duch.) cv. chandler in northern region. Int J Curr Microbiol Appl Sci 9:1633–1638

    Article  CAS  Google Scholar 

  • Kim YJ, Park HM, Cho JR, Ahn YJ (2006) Multiple resistance and biochemical mechanisms of pyridaben resistance in Tetranychus urticae. J Econ Entomol 99(3):954–958

    Article  CAS  PubMed  Google Scholar 

  • Kumral NA, Ҫobanoğlu S, Yalcin C (2010) Acaricidal, repellent and oviposition deterrent activities of Datura stramonium L. against adult Tetranychus urticae Koch. J Pest Sci 83(2):173–180

    Article  Google Scholar 

  • McMurtry JA, Croft BA (1997) Life-styles of phytoseiid mites and their roles in biological control. Annu Rev Entomol 42:291–321

    Article  CAS  PubMed  Google Scholar 

  • Nyrop J, English-Loeb G, Roda A (1998) Conservation biological control of spider mites in perennial cropping systems. In: Barbosa P (ed) Conservation Biological Control. Academic Press, San Diego, pp 307–333

    Chapter  Google Scholar 

  • Oliveira H, Fadini MAM, Venzon M, Rezende D, Rezende F, Pallini A (2009) Evaluation of the predatory mite Phytoseiulus macropilis (Acari: Phytoseiidae) as a biological control agent of the two-spotted spider mite on strawberry plants under greenhouse conditions. Exp Appl Acarol 47:275–283

    Article  PubMed  Google Scholar 

  • Opit GP, Nechols JR, Margolies DC (2004) Biological control of twospotted spider mites, Tetranychus urticae Koch (Acari: Tetranychidae), using Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseidae) on ivy geranium: assessment of predator release ratios. Biol Control 29:445–452

    Article  Google Scholar 

  • Pascua MS, Rocca M, Greco N, de Clercq P (2020) Typha angustifolia L. pollen as an alternative food for the predatory mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae). Syst. Appl. Acarol. 25(1):51–62

    Google Scholar 

  • Raworth DA (1990) Predators associated with the twospotted spider mite, Tetranychus urticae, on strawberry at Abbottsford, BC, and development of non chemical mite control. J Ent Soc Brit Columbia 87:59–67

    Google Scholar 

  • Rhodes EM, Liburd OE (2006) Evaluation of predatory mites and acramite for control of twospotted spider mites in strawberries in North Central Florida. J Econ Entomol 99:1291–1298

    Article  PubMed  Google Scholar 

  • Rhodes EM, Liburd OE, Kelts C, Rondon SI, Francis RR (2006) Comparison of single and combination treatments of Phytoseiulus persimilis, Neoseiulus californicus, and Acramite (bifenazate) for control of twospotted spider mites in strawberries. Exp Appl Acarol 39:213–225

    Article  CAS  PubMed  Google Scholar 

  • Sato ME, da Silva MZ, de Souza Filho MF, Matioli AL, Raga A (2007) Management of Tetranychus urticae (Acari: Tetranychidae) in strawberry fields with Neoseiulus californicus (Acari: Phytoseiidae) and acaricides. Exp Appl Acarol 42:107–120

    Article  PubMed  Google Scholar 

  • Scheepmaker JWA, van de Kassteele J (2011) Effects of chemical control agents and microbial biocontrol agents on numbers of non-target microbial soil organisms: a meta-analysis. Biocontrol Sci Technol 21:1225–1242

    Article  Google Scholar 

  • Strong WB, Croft BA (1995) Inoculative release of phytoseiid mites into the rapidly expanding canopy of hop for control of Tetranychus urticae Koch. Environ Entomol 24:446–453

    Article  Google Scholar 

  • Tuovinen T, Lindqvist I (2014) Effect of introductions of a predator complex on spider mites and thrips in a tunnel and an open field of pesticide-free ever bearer strawberry. J Berry Res 4:203–216

    Article  Google Scholar 

  • van de Vrie MJ, McMurtry A, Huffaker CB (1972) Ecology of tetranychid mites and their natural enemies: a review. III. Biology, ecology and pest status and host plant relations of tetranychids. Hilgardia 41:343–432

    Article  Google Scholar 

  • van Lenteren JC, Bueno VHP (2003) Augmentative biological control of arthropods in Latin America. Biocontrol 48:123–139

    Article  Google Scholar 

  • van Houten YM, Hoogerbrugge H, Bolckmans KJF (2007) Spider mite control by four phytoseiid species with different degrees of polyphagy. Integr Control Plant-Feeding Mites IOBC/wprs Bull 30(5):123–127

    Google Scholar 

  • van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40:563–572

    Article  PubMed  CAS  Google Scholar 

  • van Leeuwen T, Tirry L, Yamamoto A, Nauen R, Dermauw W (2015) The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research. Pestic Biochem Physiol 121:12–21

    Article  PubMed  CAS  Google Scholar 

  • Waite GK. Advances in the management of spider mites in field-grown strawberries in Australia. Proceedings of the Fourth International Strawberry Symposium, Tampere, Finland, July 9–14, 2002. Acta-Horticulturae 2(567)

  • Walzer A, Schausberger P (1999) Predation preferences and discrimination between con- and heterospecific prey by the phytoseiid mites Phytoseiulus persimilis and Neoseiulus californicus. Biocontrol 43:469–478

    Article  Google Scholar 

  • Xiao YF, Osborne LS, Chen JJ, McKenzie CL (2012) Functional responses and prey-stage preferences of a predatory gall midge and two predacious mites with twospotted spider mites, Tetranychus urticae, as host. J Insect Sci 13(8):1–12

    Article  Google Scholar 

  • Xu XN, Enkegaard A (2010) Prey preference of the predatory mite, Amblyseius swirskii between first instar western flower thrips Frankliniella occidentalis and nymphs of the two-spotted spider mite Tetranychus urticae. J Insect Sci 10:1–11

    Article  Google Scholar 

  • Zhang Z-Q. Mites of greenhouses. Identification, biology and control. CABI, UK. 2003. 244 pp

Download references

Acknowledgements

Not applicable.

Funding

Not applicable.

Author information

Authors and Affiliations

Authors

Contributions

The two authors conducted the research experiments (EME conducted most of the research field experiments and SFF participated in conducting the research experiments). SFF carried out the statistical analysis and constructed the figures. SFF wrote the manuscript and revised it. The two authors read and approved the final manuscript.

Corresponding author

Correspondence to Shimaa F. Fahim.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El-Saiedy, ES.M., Fahim, S.F. Evaluation of two predatory mites and acaricide to suppress Tetranychus urticae (Acari: Tetranychidae) on strawberry. Bull Natl Res Cent 45, 97 (2021). https://doi.org/10.1186/s42269-021-00558-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s42269-021-00558-2

Keywords