CONTROL OF TWO-SPOTTED SPIDER () BY A PREDATORY MITE (PHYTOSEIULUS PERSIMILIS)

Yong-Heon Kim Division of Entomology National Institute of Agricultural Science and Technology (NIAST), RDA Korea

ABSTRACT

A mass rearing technique for the predatory mite, Phytoseiulus persimilis Athias-Henriot, was successfully developed and used in five local Agricultural Extension Centers and by two commercial strawberry growers in Korea. Currently, biological control of the two-spotted , Tetranychus urticae Koch, by the predatory mite has been successfully implemented in ap- proximately 75 ha of commercial strawberry grown in vinyl greenhouses. T. urticae was effec- tively controlled by the release of predatory at a rate of 3/m2. At least two monthly re- leases were required, both for strawberry crops maturing at the normal time (February or early March) and for early-maturing crops (maturing in December and January). A schedule of abamectin plus the release of the predatory mites was compared with the application of fenazaquin. Abamectin enhanced the control of T. urticae significantly, whereas fenazaquin did not. Fenazaquin was not effective in controlling T. urticae.

INTRODUCTION Germany, it was subsequently shipped to other parts of the world, including California (McMurtry et al. In Korea, strawberry is a favorite fruit in 1978). winter and spring. Korea’s total production of Strawberries in Korea are cultivated in strawberry ranks seventh in the world. The two- greenhouses, which keep the temperature above spotted spider mite (TSM), Tetranychus urticae 5°C over the winter (October to April). Such Koch, is an extremely difficult pest to manage on temperatures are favorable for the reproduction and strawberries. The mite has become a major problem, dispersal of P. persimilis. The rate at which P. primarily because of the excessive use of pesticides. persimilis develops is a function of temperature, These kill not only TSM, but also pollinating bees in and is described by a straight line over the range of strawberry greenhouses. Pesticide use results in the temperatures between 15-30°C (Sabelis 1981). The development of strains of TSM that are highly effect of temperature on the overall predator-prey resistant to almost all classes of pesticides. In interaction was studied by Force (1967). He used addition, chemical control of TSM is highly restricted constant temperatures of 15°C, 20°C, 25°C and in Korea, because of increasing concern over 30°C, and obtained excellent control of two-spotted pesticide residues on fruits, especially on spider mites at 20°C. strawberries which are consumed fresh without Port and Scopes (1981) showed that small removal of the skin. numbers of P. persimilis could control TSM on Fortunately, the predatory mite, Phytoseiulus strawberries in walk-in plastic tunnels in southern persimilis Athias-Henriot, is now available for the England. However, it was necessary to reduce control of TSM on strawberry in Korea. This overwintering populations of TSM by introducing predacious mite was accidentally introduced into predators in the autumn. Cross (1984) showed that Germany from Chili in 1958 (Dosse 1958). From introductions of predatory mites in March or early

Key words: Phytoseiulus persimilis, Tetranychus urticae, two-spotted spider mite, biological control, strawberry, greenhouse, Korea

1 April at a rate of one mite per plant were consistently early October to mid-March, and in November and successful. Battaglia et al. (1990) studied the December they were inoculated with TSM. biological control of TSM by P. persimilis on Afterwards, populations of P. persimilis were strawberry in a greenhouse in the Metapontum area introduced onto the plants in December and January. of Italy in 1988-1989. Most of the strawberry plants used in this In 1999-2000, the effectiveness of the study broke dormancy during December, and were phytoseiid predator P. persimilis against TSM was harvested from late February onwards, although investigated in five commercial greenhouses in one experiment used an early-maturing variety. Korea. The aim of this study was to understand the Leaves of kidney bean plants infested with TSM and factors which contribute to the success or failure of P. persimilis were randomly placed on the strawberry biological control of TSM with P. persimilis on plants in the greenhouses. The P. persimilis included strawberry in Korea. all mobile stages, including nymphs. No chemicals were sprayed on the strawberry plants after the P. MASS REARING FOR RELEASE persimilis were released.

The National Institute of Agricultural Sciences Results and Technology (NIAST) in Korea, developed a mass rearing system for P. persimilis. It transferred The P. persimilis were reared in either double- this system to six local Agricultural Extension layer vinyl greenhouses or glasshouses (Table 1). Centers and two commercial strawberry growers Most of the glasshouses had problems of low relative (Table 1). The extension centers used different humidity (RH) and low temperature. The vinyl types of structures to rear P. persimilis. One center greenhouses had a higher RH but a higher incidence and a grower used a double-layer vinyl greenhouse; of disease in the kidney bean plants, the host plants four centers used glass greenhouses equipped with for TSM. In addition, the inoculation of P. persimilis warm-air heaters; the sixth used a double-layer was delayed in some greenhouses because of the vinyl greenhouse with a cloth mulch; while the poor heating system. The P. persimilis could not be second grower used a double-layer vinyl greenhouse released into three greenhouses, two of which had with a heater. The rearing space for P. persimilis warm-air heaters, because of plant damage from ranged in size from 10 to 333 m2. Kidney bean cold, a low density of TSM, or diseases in the host plants were used to rear the TSM population, a food plants. source of P. persimilis. They were cultivated from

Table 1.Transfer of the rearing technique of P. persimilis to local places and their P. persimilis release in fields, 2000

2 EFFECTIVENESS OF give good control of TSM, if one mite is released per THE BIOLOGICAL CONTROL plant when the infestation of TSM has reached two individuals per leaf, and about 30% of the leaves are Release of P. persimilis for control of infested. low densities of TSM for normal cropping season (from late February) Release of P. persimilis for control of low densities of TSM on early crops of The numbers of TSM were kept to a low level strawberry (3.4/m2) until the fruit were harvested. P. persimilis were released at the rate of 1.5/m2 on February 26, The population density of TSM on strawberry and 3/m2 on March 3 and March 10 (Fig. 1). Good plants grown for early harvest in a vinyl greenhouse control was achieved if the P. persimilis were released were < 0.1 mites/leaf in April, even after two releases while populations of TSM were still low, before of three P. persimilis/m2 in December and January their number increased. Proper timing of the release, (Fig. 2). However, TSM increased up to nine mites and numbers released, varied according to the density per m2 in the control plot. Numbers in the control of TSM, the environmental conditions such as plot fell to almost zero after spraying with abamectin. temperature and humidity, and the growth stage of Strawberry are usually harvested from February to the strawberry plants. May, but a number of growers are producing early Control is more effective if the predatory crops for export to Japan, with a harvest beginning mites are released early in the growing season. in December. For an early harvest, strawberry Waite (1988) reported that P. persimilis gave should be grown at a consistently high temperature. effective control of the pest when it was released However, high population levels of TSM can develop onto strawberry with low levels of TSM infestation very early on strawberries grown in this way. in south-east Queensland, Australia. Bonomo et al. (1991) also reported that releases of P. persimilis Release of P. persimilis after spraying gave effective control of TSM, and that it was miticides for control of high densities essential that the predator be released when the of TSM density of the pest was low (1-2 per leaf). Spicciarelli et al. (1992) recommended that phytoseiid mites If there is a high population density of TSM,

Fig. 1. Population of TSM (T. urticae) on strawberry in vinyl greenhouse after the release of P. persimilis.

3 Fig. 2. Control of TSM (T. urticae) by P. persimilis on early crop of strawberry in vinyl greenhouse. The control plot was sprayed with abamectin when the population of TSM rose to high levels.

the release of P. persimilis is more effective if following March (Table 2). Pickel et al. (1996) numbers of TSM are reduced by a chemical spray. recommended inoculative releases (i.e. initial Spraying with abamectin in January, and the release releases of a small number of predators) of P. of three P. persimilis/m2 in February, reduced the persimilis when TSM are first found in the crop. numbers of motile TSM per leaf to less than 1.0 in However, the grower in the current study released April. This indicates that the chemical application P. persimilis too late, by which time TSM had of TSM can be successfully integrated with already reached a high density. The outbreak of biological control. It seems that after about one TSM may have been caused by low humidity in month there were no hazardous residues from the May, when the weather was hot and dry. P. persimilis abamectin to harm the P. persimilis. needs a RH > 60% to survive, particularly at the egg Other pesticide sprays could also be combined stage. with the predator. The application of foliar sprays of chlorpyrifos, malathion, endosulfan, or Release of P. persimilis after biological cypermethrin, one week before or one week after control was interrupted by the applica- the introduction of P. persimilis, did not eliminate tion of a toxic chemical the predator, and resulted in successful biological control (Cross et al. 1996). Chlorpyrifos and The most common reason for the failure of the malathion were also successful, but a longer time biological control of TSM is the application of was needed after spraying before the predator was nonselective pesticides. P. persimilis is very introduced. Trumble and Morese (1993) reported susceptible to almost all chemical pesticides. When that the best economic returns were generated by P. persimilis was released at the rate of 1.5/m2 in abamectin in combination with P. persimilis. February and 3/m2 in March, the crop was then sprayed with fenazaquin. This pesticide seems to be Release of P. persimilis to control high toxic to P. persimilis, and the population densities densities of TSM late in the cropping of TSM rose to 13.8/leaf in April (Fig. 4). Population season densities of TSM then fell after spraying with milbemectin later that month. Subsequently, the The population densities of TSM per leaf grower stopped using P. persimilis and sprayed increased to 11.3 in February and 33.3 in March, chemicals instead. while the percentage of leaves infested with TSM Many growers who have not had any increased from 36.7% in December to 71.5% the experience of using predatory mites are doubtful

4 Fig. 3. Control of TSM (T. urticae) on strawberry in vinyl greenhouse by a chemical spray followed by the release of P. persimilis.

Table 2.Control of TSM (T. urticae) on strawberry in vinyl greenhouse by P. persimilis*, released when numbers of TSM were high

Fig. 4. Control of TSM (T. urticae) on strawberry in vinyl greenhouse by mibemectin, after biological control was interrupted by the application of fenazaquin

5 whether P. persimilis is an effective control agent Cross, J.V., C.M. Burgess, and G.R. Hanks. against TSM. As the resistance of TSM to chemicals 1996. Integrating insecticide use with such as fenazaquin increases, TSM becomes able to biological control of two spotted spider survive chemical applications. However, natural mite (Tetranychus urticae) by Phytoseiulus enemies, including P. persimilis, are also highly persimilis on strawberry in the UK. In: susceptible to these chemicals. Proceedings, Brighton Crop Protection Conference on Pest and Diseases. Vol. 3, CONCLUSION pp. 899-906. Dosse, G. 1958. Über einige neue It would appear that P. persimilis can give Raubmibenarten (Acar., ). good control of two-spotted spider mite on Pflanzenschutzber. 21: 44-61. strawberry crops, particularly if the predator is Force, D.C. 1967. Effect of temperature on introduced early in the cropping season when biological control of two-spotted spider numbers of TSM are still fairly small. If it is mites by Phytoseiulus persimilis. Jour. introduced into dense populations of TSM, the Econ. Entomol. 60: 1308-11. control effect is limited. In this situation, it is best McMurtry, J.A., E.R. Oatman, P.A. Phillips, to spray a miticide to reduce the numbers of TSM. and C.W. Wood. 1978. Establishment If abamectin is used, or foliar sprays of chlorpyrifos, of Phytoseiulus persimilis (: malathion, endosulfan or cypermethgrin, P. Phytoseiidae) in southern California. persimilis can be introduced a week after spraying Entomophaga 23: 175-79. with no harmful effects on the predator. Other Pickel, C., P. Phillips, J.Trumble, N. Welch, pesticides may need a longer waiting period after and F. Zlom. 1996. IPM Pest spraying. One study found that a combination of Management Guidelines: Strawberry. UC abamectin and P. persimilis was the most cost- DANR Publication 3339. effective way of controlling TSM in greenhouses. Post, C.M. and N.E.A. 1981. Biological However, pesticides must be selective, because P. control by predatory mites (Phytoseiulus persimilis is susceptible to almost all chemical sprays. persimilis Athias-Henriot) of red spider mite (Tetranychus urticae Koch) infesting strawberries in “walk-in plastic tunnels. REFERENCES Plant Pathology 30: 95-99. Sabelis, M.W. 1981. Biological Control of Battablia, D., Borriello, and R. Spicciarelli. Two-spotted Spider Mites using Phytoseiid 1990. Biological control Tetranychus Predators. Part 1. Modelling the urticae Koch by Phytoseiulus persimilis Predator-prey Interaction at the Individual Athias-Henriot on protected strawberry in Level. Centre for Agricultural Publishing the Metapontum area. Informatore- and Documentation, Wageningen. 242 pp. fitopatologico 40: 44-46. Spicciarelli, R.D. Battaglia, and A. Bonomo, G., G. Catalano, V. Maltese, and S. Tranfaglia. 1992. Biological control of Sparta. 1991. Biological and integrated Tetranychus urticae with Phytoseiulus control experiments in Marsalese persimilis on strawberry. Informatore strawberry crops. Infromatore Agrario Agrario 48,11: 59-62. 47: 97-100. Trumble, J.T. and J.P. Morse. 1993. Cross, J.V. 1984. Biological control of two- Economics of integrating the predaceous spotted spider mite (Tetranychus urticae) mite Phytoseiulus persimilis (Acari: by Phytoseiulus persimilis on strawberries Phytoseiidae) with pesticides in grown in “walk-in” plastic tunnels, and a strawberries. Horticultural Entomology 86: simplified method of spider mite 879-885. population assessment. Plant Pathology Waite, G.K. 1998. Integrated control of 33: 417-423. Tetranychus urticae in strawberries in Southeast Queensland. Experimental and Applied Acarology 5: 23-32.

6