Effectiveness of Huwa-San TR50 on Tomato Russet Mite Aculops lycopersici (Massee) (Acari: Eriophyideae)

Mahmoud M. Al-Azzazy1,2 and Saleh S. Alhewairini1,*

1Department of Plant Production and Protection, College of Agriculture and Veterinary Medicine, Qassim University, P.O. Box 6622, Buraidah 51452, Al-Qassim, Saudi Arabia

2Agricultural Zoology and Nematology Department, Faculty of Agriculture, Al-Azhar University, Cairo, Egypt

ABSTRACT

This study evaluated the effectiveness of Huwa-San TR50 against all stages of Aculops lycopersici. This includes its side effects on the associated predatory mite, Neosiulus cucumeris. Huwa-San TR50 is a formulation of hydrogen peroxide, stabilized by the addition of a small quantity of silver and is extensively used as a disinfectant. It was found to be very effective in killing A. lycopersici with no significant effect on N. cucumeris. Under greenhouse conditions, the mortality percentages were 81.17, 84.11, 92.74 and 95.10% for A. lycopersici and 15.86, 23.45, 33.33 and 58.19% for N. cucumeris after one week of exposure to 1000, 2000, 3000 and 4000ppm of Huwa-San TR50, respectively. Under laboratory conditions, the mortality percentages were 83.24, 85.13, 94.21 and 97.36% for A. lycopersici and 17.14, 27.55, 37.14 and 59.37% for N. cucumeris at 1000, 2000, 3000 and 4000 ppm of Huwa-San TR50, respectively. In addition, Huwa-San TR50 caused a concentration dependent reduction in the percentage of egg hatching. The percentages of larvae hatching from eggs of A. lycopersici were 73.42, 56.92, 25.41 and 17.97 under greenhouse conditions and 68, 53.14, 23.51 and 15.18 under laboratory conditions at 1000, 2000, 3000 and 4000ppm of Huwa-San TR50 after one week of treatment compared with the control (well water), respectively. The application of Huwa-San TR50 showed a promising safety profile when compared to other acaricides, as it spared predatory mites at concentrations which had a high lethality to tomato russet mites. Hence, Huwa-San TR50 can be utilized in the Integrated Pest Management (IPM) program as an acaricide agent.

Article Information

Received 07 October 2017

Revised 27 November 2017

Accepted 12 December 2017

Available online 11 April 2018

Authors’ Contribution

SSA and MMA equally contributed in designing experiment, analyzing the collected data and writing the manuscript.

Key words

Huwa-San TR50, Tomato russet mite, Aculops lycopersici, Neosiulus cucumeris.

DOI: http://dx.doi.org/10.17582/journal.pjz/2018.50.3.869.875

* Corresponding author: hoierieny@qu.edu.sa

0030-9923/2018/0003-0869 $ 9.00/0

Introduction

Tomato russet mite (TRM), Aculops lycopersici (Massee) (Acari: Eriophyideae) was first described in Australia by Massee (1937). Thereafter, it was recorded on tomato plants in several countries such as Korea (Kim et al., 2002), USA (Anderson, 1954), Egypt (Abou-Awad, 1979), Argentina (Rossi, 1962), Brazil (Fletchman and Aranda, 1970), Venezuela (Cermeu et al., 1982), Japan (Nemoto, 2000) and Saudi Arabia (Gentry, 1965; Martin, 1971; EPPO, 2014). It was considered as an important pest of tomato (Solanum lycopersicum L.) because it can cause serious damage to tomato plants. Its infestations cause destruction of the epidermal cells of the leaflet leading to a curling of the leaflet edges, desiccation, tissue damage and plant death (Keifer et al., 1982; Royalty and Perring, 1988; Haque and Kawai, 2002). It can also rust or cross-crack the surface of fruits (Kim et al., 2002). Moreover, there are more than 24 host plants of A. lycopersici distributed in three different plant families Solanaceae, Convolvulaceae and Rosaceae (Perring, 1996; Larrain, 2000; Duso et al., 2010).

The efficacy of several insecticides and/or acaricides against A. lycopersici has been tested. For example, Abou-Awad and El-Banhawy (1985) evaluated the susceptibility of A. lycopersici to methamidophos, pyridaphenthion, cypermethrin, dicofol and fenarimol. In addition, Royalty and Perring (1987) compared the toxicity of five acaricides namely avermectin B1, dicofol, cyhexatin, sulfur, and thuringiensin to A. lycopersici. Kashyap et al. (2014) tested the efficacy of abamectin, azadirachtin, spiromesifen, mineral oil and hexythiazox against A. lycopersici.

In comparison with mite species belonging to Tetranychidae, Eriophyoid mites showed equal susceptibility to many acaricides such as amitraz, dicofol, propargite, ethion, bromopropylate and abamectin (Thomas et al., 2009). However, Tetranychidae suffered few effects from benzoylphenylurea insecticides diflubenzuron and teflubenzuron whereas russet mites were adversely affected (Childers et al., 1996; Scarpellini and Clari, 1999). Despite the high susceptibility of Eriophyoid mites to most available acaricides, several species of Eriophyoid mites (including A. lycopersici) have developed resistance. In Egypt for example, the resistance of A. lycopersici to methamidophos was reported after three seasons of use (Abou-Awad and El-Banhawy, 1985). This would encourage scientific researchers to find alternative strategies for controlling A. lycopersici.

Little information has been published on the control of A. lycopersici and Huwa-San TR50 has not been considered for use against this species of mite. Alhewairini (2017) was the first to report that Huwa-San TR50 can be used as an insecticide in controlling cotton aphids (Aphis gossypii Glover) without significant effects on honeybees (Apis mellifera lamarckii) and seven-spot ladybird beetles (Coccinella septempunctata). Moreover, Alhewairini and Al-Azzazy (2017a, b, c) were the first to document that Huwa-San TR50 has acaricidal activity as it can successfully kill two spotted spider mites (Tetranychus urticae Koch) with minimal effects on its associated predatory mite, (Neosiulus cucumeris), Varroa mite (Varroa jacobsoni Oudemans) and the date palm mite, Oligonychus afrasiaticus (McGregor).

Huwa-San TR50 is widely used as a disinfectant and was developed over twenty years ago (www.huwasan.com). It is a formulation of hydrogen peroxide which has been stabilized by the addition of a small quantity of silver (www.huwasan.com). Furthermore, it has several advantages that make it reliable and safe, such as its high efficacy even at low concentrations, being effective under a wide range of temperatures up to boiling point, being gentle to the skin, having long term effectiveness, being biodegradable, having no build-up of resistance by microorganisms, as well as being non-toxic to humans, colorless, tasteless and odorless (www.huwasan.com).

This study evaluated the effectiveness of Huwa-San TR50 against A. lycopersici and its secondary effects on the associated predatory, N. cucumeris under greenhouse and laboratory conditions.

Materials and methods

Solutions and experiment protocol

Huwa-San TR50 was obtained from Ghatafan Company in Onaizah (retailer agent). The field experiments were carried out at the Experimental Research Station, Qassim University, Buraidah, Al-Qassim, Saudi Arabia under greenhouse conditions during the May 2017 season in an abandoned tomato (Solanum lycopersicum L.) greenhouse, having a history of tomato russet mite infestations. The stock solution of Huwa-San TR50 (500,000 ppm) was diluted with well water to give a serial concentration range between 1000 to 4000 ppm.

About 10 m2of cultivated land with tomato seedlings (Pritchard cultivar) was chosen and divided into 5 plots (each plot was about 2 m2), and all plots were arranged using a randomized complete block design. Ten tomato leaves of each treatment were randomly collected and placed in a clean labeled plastic bag and transported to the laboratory to determine the initial density and distribution of A. lycopersici and N. cucumeris (moving stages and eggs) as a pre-spray count using a stereomicroscope. Under greenhouse conditions, four different concentrations 1000, 2000, 3000 and 4000 ppm of Huwa-San TR50 including control (well water) with 5 replicates were directly sprayed on the tomato plants (heavily infested by tomato russet mite) using a knapsack sprayer (20 L).

Direct observations were made one week after the application of four Huwa-San TR50 concentrations, by using a stereomicroscope to determine the percentage reduction in the population of tomato russet mites on the tomato plants after spraying.

The laboratory experiments were conducted in a laboratory (25±2ºC and 70% relative humidity). Non-treated tomato leaves (heavily infested by tomato russet mite) were randomly collected and placed in a clean plastic bag and then transferred to the Department of Plant Production and Protection, College of Agriculture and Veterinary Medicine, Qassim University for immediate bioassay. The collected tomato leaves were arranged in a randomized complete block design.

Wet cotton, 4.0 cm in diameter, was used as rearing arenas in plastic Petri-dishes (5 × 1 cm) with the lower surface of leaves facing upwards. The cotton bed was kept wet by soaking with distilled water twice daily to keep the leaf discs fresh and to avoid the migration of mites to the lower leaf surface. The leaf discs were checked under a stereomicroscope to ensure that no other predatory insects and mites were present. To determine pre-spray counts, the number of A. lycopersici and N. cucumeris (moving stages and eggs) was manually counted by direct observation under a stereomicroscope. Thereafter, four different concentrations 1000, 2000, 3000 and 4000 ppm of Huwa-San TR50 including control (well water) with 5 replicates were sprayed directly on the Petri-dishes by using a small knapsack sprayer (1L). Dead mites were counted one week after applying control (well water) and four concentrations of Huwa-San TR50 to determine the percentage mortality.

Statistical analysis

The percentage reduction in the average populations of tomato russet mite (A. lycopersici) and the predatory mite (N. cucumeris Oudemans) were calculated using the equation of Henderson and Tilton (1955).

Where, n is number of A. lycopersici and N. cucumeris population, T is treated, Co is control and Tr is treatment.

The mortalities of A. lycopersici and N. cucumeris were calculated manually by direct observation under a stereomicroscope. Thereafter, the average percentage of a number of larvae hatching from eggs was calculated by using Microsoft Excel Program. All variables of the obtained data were statistically analyzed using One-way analysis of variance (ANOVA). Curves for the mortality assays and number of larvae hatching from eggs were plotted using Graphpad Prism version 7. The data points were the mean ± SEM of each treatment with Huwa-San TR50 and the graphs were fitted using a non-linear regression (log (inhibitor) vs. normalized response- variable slope) with a four parameter logistic equation with a maximum and a minimum plateau. The results are expressed as mean mortality percentage ± SEM for each treatment.

Results

The obtained results showed the effectiveness of Huwa-San TR50 against all stages of A. lycopersici including eggs with a minimal effect on the mortality of the associated predatory N. cucumeris.

Under greenhouse conditions, the mortality percentages were 81.17, 84.11, 92.74 and 95.10% for A. lycopersici and 15.86, 23.45, 33.33 and 58.19% for N. cucumeris one week after exposure to 1000, 2000, 3000 and 4000 ppm of Huwa-San TR50, respectively (Tables I, II). Under laboratory conditions, the mortality percentages were 83.24, 85.13, 94.21 and 97.36% for A. lycopersici and 17.14, 27.55, 37.14 and 59.37% for N. cucumeris at 1000, 2000, 3000 and 4000 ppm of Huwa-San TR50, respectively (Tables I, II). The maximum mortality (> 95%) was obtained after exposure to 4000 ppm of Huwa-San TR50; although the difference between 3000 and 4000 ppm of Huwa-San TR50 on the mortality of A. lycopersici was statistically insignificant in both conditions (greenhouse and laboratory) (Table I). Clearly, Huwa-San TR50 affects the color of the eggs and cuticle of adult A. lycopersici, by changing them to light brown from white and by inducing malformation of the eggs and the cuticle of the adult.

Table I.- Effect of four concentrations of Huwa-San TR50 on tomato russet mite Aculops lycopersici (Massee) (Acari: Eriophyideae) infested tomato plants under greenhouse and laboratory conditions.

Concentration (ppm)	No. of mites/leaf
	Under greenhouse conditions			Under laboratory conditions
	Pre-spray count	Average post-spray count *	Reduction (%)**	Pre-spray count	Average post-spray count *	Reduction (%) **
Control	101.14	99.23	0.00 a	88.56	87.45	0.00 a
1000	104.85	18.24	81.17 b	87.45	14.82	83.24 b
2000	90.11	14.58	84.11 b	82.64	12.37	85.13 b
3000	102.78	8.13	92.74 c	91.69	5.28	94.21 c
4000	98.71	4.02	95.10 c	86.38	2.52	97.36 c

*Counts made one week post treatment. ** Mortality values calculated with the Henderson-Tilton equation. Mean followed by the same letter in a column are not significantly different from each other at P>0.05.

Table II.- Corrected mortality percentage of the predatory mite, Neosiulus cucumeris Oudemans (Acari: Phytoseiidae) associated with tomato plants treated with four concentrations of Huwa-San TR50 under greenhouse and laboratory conditions.

Concentration (ppm)	No. of predatory mites/leaf
	Under greenhouse conditions			Under laboratory conditions
	Pre-spray count	Average post-spray count*	Reduction (%)**	Pre-spray count	Average post-spray count*	Reduction (%)**
Control	5.12	5.25	0.00 a	4.98	4.89	0.00 a
1000	5.73	4.81	15.86 b	4.55	3.77	17.14 b
2000	6.13	4.66	23.45 c	4.56	3.29	27.55 c
3000	6.03	4.00	33.33 d	5.17	3.21	37.14 d
4000	5.81	2.41	58.19 e	5.88	2.31	59.37 e

*Counts made one week post treatment. ** Mortality values calculated with the Henderson-Tilton equation. Mean followed by the different letter in a column are significantly different from each other at P<0.05.

Table III.- Number of larvae hatching from eggs of the tomato russet mite Aculops lycopersici (Massee) (Acari: Eriophyideae) treated with four concentrations of Huwa-San TR50 under greenhouse and laboratory conditions.

Concentration (ppm)	No. of eggs and larvae /leaf
	Under greenhouse conditions			Under laboratory conditions
	No. of eggs pre-spray count	Average number of larvae post-spray count*	Hatching (%) **	No. of eggs pre-spray count	Average number of larvae post-spray count*	Hatching (%) **
Control	34.45	34.22	0.00 a	36.78	35.67	0.00 a
1000	34.36	25.23	73.42 b	35.47	24.12	68.00 b
2000	36.87	20.99	56.92 c	37.18	19.76	53.14 c
3000	39.82	10.12	25.41 d	35.17	8.27	23.51 d
4000	40.28	7.24	17.97 e	34.58	5.25	15.18e

*Counts made one week post treatment. ** Hatching percentage calculated with Microsoft Excel program. Mean followed by the different letter in a column are significantly different from each other at P<0.05.

There was no significant difference between the two conditions (greenhouse and laboratory) on the mortality of A. lycopersici (P = 0.713 by using F-test in Graphpad Prism 7) and the predatory mite, N. cucumeris, (P = 0.623 by using F-test in Graphpad Prism 7) after one week of exposure to Huwa-San TR50 at all concentrations used (Fig. 3). However, the difference between tomato russet mite (A. lycopersici) and the predatory mite (N. cucumeris Oudemans) at the two conditions (greenhouse and laboratory) was significant (P < 0.01 by using F-test in Graphpad Prism 7) (Fig. 1).

The percentages of larvae hatching from the eggs of A. lycopersici were 73.42, 56.92, 25.41 and 17.97 under greenhouse conditions and 68, 53.14, 23.51 and 15.18 under laboratory conditions at 1000, 2000, 3000 and 4000 ppm of Huwa-San TR50 after one week of treatment compared with control (well water), respectively (Table III).

Discussion

Unfortunately, many acaris including A. lycopersicican sustain their population and become insensitive to the regular application of most available acaricides due to their resistance to these acaricidal agents. Researchers are interested in finding alternative acaricidal agents that can effectively be used in controlling A. lycopersici. Therefore, this study was designed to test the effectiveness of Huwa-San TR50 against the adult and eggs of A. lycopersici including its side effects on the associated predatory mite, N. cucumeris under both greenhouse and laboratory conditions.

The laboratory results of this study showed that the application of Huwa-San TR50 caused serious damage to the cuticle of A. lycopersici. Its application can also turn the eggs and cuticle color of adult A. lycopersici to from white to light brown as well as causing malformation of the egg shape and adult cuticle. This damage resulted in the death of A. lycopersici and a failure in the hatching of eggs. These findings are consistent with previous findings already reported by Alhewairini and Al-Azzazy (2017a, b, c). Huwa-San TR50 showed the same damage symptoms on the cuticle of A. lycopersici which were already seen on two spotted spider mites (T. urticae), Varroa mite (V. jacobsoni) and the date palm mite (O. afrasiaticus). Moreover, similar damage to the cuticle were seen on cotton aphids (A. gossypii) (Alhewairini, 2017) and after the application of a certain concentration of Huwa-San TR50.

More than 99% mortality of A. lycopersici was achieved by applying azadirachtin, spiromesifen, mineral oil, hexythiazox and abamectin (Kashyap et al., 2014). The latter was the most toxic among these acaricides. In comparison with this statement, 3000 ppm of Huwa-San TR50was reported to be safe to tomato leaves (Alhewairini and Al-Azzazy, 2017a). At this concentration, 95.10% of A. lycopersici was killed and only 25.41% of the exposed eggs were successfully hatched. Clearly, Huwa-San TR50 seems capable of disrupting the eggs hatching of A. lycopersici, because the exposed eggs failed to hatch when the concentration of Huwa-San TR50 was increased (Table II; Fig. 2).

Interestingly, 3000 ppm had an insignificant effect on the mortality of the associated predatory mite, N. cucumeris (< 33%); although it was exposed to Huwa-San TR50 by direct application on treated A. lycopersici. This emphasizes the selectivity of Huwa-San TR50 against both the adult and eggs of A. lycopersici. Furthermore, 3000 ppm of Huwa-San TR50 was less toxic to the predatory mite, N. cucumeris by about 24% compared with 4000 ppm under both conditions (greenhouse and laboratory). Therefore, there is no need to exceed 3000 ppm of Huwa-San TR50 when controlling A. lycopersici, since leaf malformation of tomato plants was already registered beyond this concentration (Alhewairini and Al-Azzazy, 2017a). In contrast, abamectin was found to be highly toxic to both predatory mites (Neosiulus californicus and Phytoseiulus macropilis) and produced mortalities of 60 and 85% after 72 h, respectively (Bernardi et al., 2012). Therefore, the control of A. lycopersici with Huwa-San TR50 would most unlikely reduce the population number of the associated predatory mite, N. cucumeris compared with most available acaricides.

The results obtained are consistent with our previous results as Huwa-San TR50 was found to be very safe to predatory mite, N. cucumeris (Alhewairini and Al-Azzazy, 2017a). In another study, Huwa-San TR50 was also non-toxic to beneficial insects such as honeybees (Apis mellifera lamarckii) up to 4000 ppm and seven-spot ladybird beetles (Coccinella septempunctata) up to 3000 ppm (Alhewairini, 2017). This means that Huwa-San TR50 can effectively kill and cause a failure in egg hatching of A. lycopersici with insignificant effect on the number of predatory mite and insects.

Finally, Huwa-San TR50 provided an effective suppression of A. lycopersici population as it can effectively kill and produce a failure in the eggs hatching of A. lycopersici under both greenhouse and laboratory conditions.

Conclusion

This study has determined a new target organism that can be effectively killed by the application of Huwa-San TR50. The application of Huwa-San TR50causes damage to the cuticle of A. lycopersici leading to the death of this mite. This includes its ability to reduce the number of larvae hatching from eggs which can help in achieving successful control by reducing the mite population. Further research is encouraged to investigate the mode of action of Huwa-San TR50 on the cuticle of tomato russet mite (A. lycopersici). The application of Huwa-San TR50 showed a promising safety profile when compared to other acaricides, since it spared a reasonable number of predatory mites. Hence, Huwa-San TR50 can be used in the IPM program as an acaricidal agent.

Acknowledgements

The authors gratefully acknowledge Qassim University, represented by the Deanship of Scientific Research, for the material support of this research under the number (3046) during the academic year 1436 AH / 2015 AD. The authors wish to acknowledge Dr. Mohamed Motawei and Dr. Mohammad Al-Deghairi for revising this manuscript.

Statement of conflict of interest

The authors declare that there is no conflict of interest.

References

Abou-Awad, B.A., 1979. Über die Rotgelbe Tomatenmilbe, Aculops lycopersici (Massee) (Acari, Eriophyidae), in Ägypten. Anz. Schädlingskd., Pflanz. Umweltschutz, 52: 153-156.

Abou-Awad, B.A. and El-Banhawy, E.M., 1985. Susceptibility of the tomato russet mite, Aculops lycopersici in Egypt to methamidiphos, pyridaphenthion, cypermethrin, dicofol and fenarimol. Exp. appl. Acarol., 1: 11-15. https://doi.org/10.1007/BF01262195

Alhewairini, S.S., 2017. Innovative approach for the use of Huwa-San TR50 in controlling cotton aphids (Aphis gossypii Glover). J. agric. Sci., 9: 77. https://doi.org/10.5539/jas.v9n4p77

Alhewairini, S. and Al-Azzazy, M., 2017a. Innovative approach for the use of Huwa-San TR50 in controlling two spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae). Pakistan J. Zool., 50: 241-247.

Alhewairini, S. and Al-Azzazy, M., 2017b. Innovative approach for controlling Varroa jacobsoni Oudemans (Acari: Varroidae) using Huwa-San TR50 on honeybees Apis mellifera. J. Fd. Agric. Environ., 15: 88-91.

Alhewairini, S. and Al-Azzazy, M., 2017c. A new approach for controlling the date palm mite, Oligonychus afrasiaticus (McGregor) (Acari: Tetranychidae) using Huwa-San TR50. J. Fd. Agric. Environ., 15: 63-67.

Anderson, L.D., 1954. The tomato russet mite in the United States. J. econ. Ent., 47: 1001-1005.

Bernardi, D., Botton, M., da Cunha, U.S., Bernardi, O., Malausa, T., Garcia, M.S. and Nava, D.E., 2012. Effects of azadirachtin on Tetranychus urticae (Acari: Tetranychidae) and its compatibility with predatory mites (Acari: Phytoseiidae) on strawberry. Pest. Manage. Sci., 69: 75-80. https://doi.org/10.1002/ps.3364

Cermeu, M., Doreste, S.E. and Van Balen, L., 1982. Aculops lycopersici (Massee 1937) (Acari: Eriophyidae) plaga del cultivo del tomate en Venezuela. Rev. Fac. Agron., 12: 227-234.