Efficacy of different release strategies of Neoseiulus

Systematic & Applied Acarology (2002) 7, 000-000

ISSN 1362-1971

Efficacy of different release strategies of Neoseiulus californicus McGregor and Phytoseiulus persimilis Athias Henriot (Acari: Phytoseiidae) for the control of two-spotted spider mite (Tetranychus urticae Koch) on greenhouse cut roses SYLVIA BLÜMEL & ANDREAS WALZER Federal Office and Research Centre for Agriculture, Institute of Phytomedicine Spargelfeldstr. 191, A-1226 Vienna, Austria

Abstract Separate and combined releases of P. persimilis and N. californicus were tested for the control of T. urticae on greenhouse cut roses under integrated pest management conditions. Release strategies were carried out in separate greenhouses and were not replicated. Mite densities were controlled at regular intervals on 50 single, randomly collected leaves per greenhouse. Naturally infestations of 23.9 T. urticae per leaf at the start of the trial were controlled throughout the growing season by the simultaneous, combined release of 26 P. persimilis/ m² and 24 N. californicus/ m² in total. Separate releases of each phytoseiid species - 32 P. persimilis/m² in total at an initial infestation of 0.16 T. urticae per leaf, or 51 N. californicus/m² in total at a an initial infestation of 10.2 T. urticae per leaf - failured to adequately suppress spider mite populations. Additional treatments with selective acaricides were required. Reasons for the different control success of the three release strategies and their implications for practical use are discussed. Key words: greenhouse roses, biological control, integrated control, Tetranychus urticae, Phytoseiulus persimilis, Neoseiulus californicus

Introduction The two spotted spider mite Tetranychus urticae Koch (Acari, Tetranychidae) is considered as one of the most important pests of roses in greenhouses (Van de Vrie 1985). As chemical control measures turned out increasingly inefficient, integrated and biological pest management were proposed as alternative strategies. For biological and integrated control of tetranychid mites on greenhouse roses separate releases of different phytoseiid species have been evaluated with varying degrees of success (Simmonds 1972; Hamlen & Lindquist 1981; Burgess 1984; Field & Hoy 1986; Blümel 1990; Gough 1991). The most frequently used predatory mite was Phytoseiulus persimilis Athias-Henriot (Acari, Phytoseiidae), which is a specialist predator of spider mites producing dense webbing (McMurtry & Croft 1997). With regard to the requirements for successful spider mite control, advantageous traits of P. persimilis are a high predation rate, a high reproduction rate, a short developmental cycle and a great searching capacity (McMurtry & Croft 1997). These traits enable P. persimilis to rapidly suppress T. urticae populations on greenhouse roses (Simmonds 1972; Burgess 1984; Blümel 1990; Zhang & Sanderson 1995). A disadvantage of P. persimilis for biocontrol is its failure to persist at low or diminishing prey densities - primarily due to its narrow food range -, which interferes with long term, sustainable control strategies (Sabelis 1985; McMurtry & Croft 1997). This allows only curative releases of P. persimilis after T. urticae infestations are © 2002 Systematic & Applied Acarology Society

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present and already established on the plants, thus risking the occurrence of plant damage above an economic threshold level. From experimental evidence a combined release of a specialist predator and a generalist predator may complement each other, which should result in both rapid suppression and long-term control of spider mites (Mori & Saito 1979; Croft & McRae 1992 a,b). The phytoseiid Neoseiulus californicus McGregor (Acari, Phytoseiidae) seems to be a promising candidate for the combined release with P. persimilis. Neoseiulus californicus is used for biological control of spider mites in various field crops (McMurtry & Croft 1997) and specific greenhouse crops (Calvitti & Tsolakis 1992; Smith et al. 1993), but exhibits lower functional and numerical responses to T. urticae than does P. persimilis (Friese & Gilstrap 1982; Gilstrap & Friese 1985). However, permanent establishment may be facilitated by the broad food range of N. californicus, which can survive and reproduce on different mite and insect species and pollen (Swirskii et al. 1970; Castagnoli & Falchini 1993; Croft et al. 1998), although it shows a preference for spider mites (McMurtry & Croft 1997). Additionally, N. californicus seems to be more tolerant to pesticides than P. persimilis (Croft et al. 1976; Blümel 1999), which should facilitate its survival during commercial integrated crop production. In contrast to P. persimilis, overwintering and unassisted reestablishment of N. californicus in the following spring is possible due to the ability (Castagnoli et al., 1994; Schöntag 1999) to diapause. The effects of possible interactions between both phytoseiid species, which were already found in extensive laboratory studies (Walzer & Schausberger 1999 a,b; Walzer & Blümel 1999) also have to be considered. A small-scale, short-term study showed that P. persimilis is implicitly superior in competition for food, but is inferior in intraguild predation to N. californicus. Consequently, P. persimilis was dominant at high spider mite densities, whereas N. californicus outcompeted P. persimilis at diminishing spider mite densities and persisted until the end of the experiment (Schausberger & Walzer 2001). However, long-term studies in commercial greenhouses under practical conditions are still lacking. The aim of the present study was to investigate the efficacy of the combined release of P. persimilis and N. californicus to control T. urticae on cut roses under practical conditions, with an emphasis on the long-term effect of spider mite control. The phytoseiids were released either separately or simultaneously in combination in commercial greenhouses.

Materials and Methods The trials were conducted simultaneously in three parallel situated greenhouses of a commercial cut rose producer, which contained test plants of the rose variety ”First Red” (Table 1). The roses were produced in single pots (three rose plants per pot) filled with peat, which were placed on plastic cover on the soil and connected to a closed drip irrigation and fertiliser system. Roses were produced the whole year round, but included a resting and cleaning phase with minimum temperatures adjusted to 8–10 °C, from mid December until mid January, during which old foliage was removed and the plants were pruned. No additional light was given. The rose variety ”First Red” was shown to be susceptible to spider mite infestation in previous laboratory and small scale greenhouse trials and was suitable for P. persimilis and N. californicus (Walzer 1998). From the beginning of February until mid March the minimum temperature was increased and adjusted to 15°C by the computerised climate regulator. Temperature and relative humidity were recorded daily. Plant training by the grower followed standard horticultural practice. The trial lasted from the middle of March, when spider mite infestation was earliest visible, to the middle of September 1998.

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TABLE 1: Trial parameters Criteria

Greenhouse 1

Greenhouse 2

Greenhouse 3

Size

626 m²

626 m²

855 m²

Rose variety

”First Red” 8 rows



”Kiss” 8 rows

”Safari” 2 rows ”Confetti” 4 rows

Introduction rate (predatory mites) in total/m² frequency

51 N. californicus/m²

26 P. persimilis/m²+ 24 N. californicus/m²

32 P. persimilis/m²

11 releases

9 releases

8 releases

chemical treatment during the trial* T. urticae

2 x Acorit fl. 0.05%

/

2 x Acorit fl. 0.05%

Aphids (Macrosiphum euphorbiae, Rhodobium porosum)

2x Pirimor DG 0.05% 4x Phosdrin EC 0.1%

2x Pirimor DG 0.05% 3x Phosdrin EC 0.1% 1x Unden fl. 0.2%

2x Pirimor DG 0.05% 3x Phosdrin EC 0.1% 1x Unden fl. 0.2%

Thrips (Frankliniella occidentalis and other species)

1x Phosdrin EC 0.1%

/

1x Phosdrin EC 0.1%

Powdery mildew (Spaerotheca pannosa)

7x Meltatox 0.2% 5x Prothane 0.03% 3x Discus 0.02% 2x Condor 0.012% 1x Saprol EC 0.15% 1x Baymat fl. 0.1%

7x Meltatox 0.2% 6x Prothane 0.03% 3 x Discus 0.02% 2x Condor 0.012% 1x Saprol EC 0.15% 1x Provin 0.1%

9x Meltatox 0.2% 5x Prothane 0.03% 3x Discus 0.02% 2x Condor 0.012% 1x Baymat fl. 0.1%

Trial period

19.03.1998 - 15.09.1998

* Active ingredients of listed plant protection products Plant protection products Active ingredients (amount per kg or l) Acorit flüssig Phosdrin EC

Hexythiazox 100 gl-1 Mevinphos 96 gl-1 Pirimicarb 500 gkg-1

Pirimor DG Unden flüssig

Propxur 202 gl-1

Baymat flüssig

Biertanol 300 gl-1

Condor

Triflumizole 500 gkg-1

Discus

Kresoxim-methyl 500 gl-1

Meltatox

Dodemorph 317 gl-1

Prothane

Myclobutanil 125 gl-1

Provin

Chlorthalonil 720 gl-1

Saprol Neu

2002

Triforine 190 gl-1

BLÜMEL & WALZER: INTEGRATED CONTROL OF SPIDER MITED ON ROSES

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A

A

30.0

a

20.0

10.0

0.0 19.3. 2.4. 16.4. 30.4. 14.5. 28.5. 11.6. 25.6. 9.7. 23.7. 6.8. 20.8. 3.9. 17.9.

A

A

Mean number of mites per leaf

5.0

b 4.0 3.0 2.0 1.0 0.0 19.3. 2.4. 16.4. 30.4. 14.5. 28.5. 11.6. 25.6. 9.7. 23.7. 6.8. 20.8. 3.9. 17.9.

A

A

c

5.0 4.0 3.0 2.0 1.0 0.0 19.3.

16.4.

14.5.

11.6.

9.7.

6.8.

3.9.

FIGURE 1. Population development of T. urticae (= a), P. persimilis (= b) and N. californicus (= c) in greenhouse with release of N. californicus. A = Acorit 0.05%. Adult, juveniles and eggs are represented by black, grey and white bars respectively (square root transformed data).

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A

A

a

30.0

20.0

10.0

0.0 19.3. 2.4. 16.4. 30.4. 14.5. 28.5. 11.6. 25.6. 9.7. 23.7. 6.8. 20.8. 3.9. 17.9.

A

A

b


5.0 4.0 3.0 2.0 1.0 0.0 19.3. 2.4. 16.4. 30.4. 14.5. 28.5. 11.6. 25.6. 9.7. 23.7. 6.8. 20.8. 3.9. 17.9.

A

A

5.0

c 4.0 3.0 2.0 1.0 0.0 19.3. 2.4. 16.4. 30.4. 14.5. 28.5. 11.6. 25.6. 9.7. 23.7. 6.8. 20.8. 3.9. 17.9.

FIGURE 2. Population development of T. urticae (= a), P. persimilis (= b) and N. californicus (= c) in greenhouse with release of P. persimilis A = Acorit 0.05%. Adult, juveniles and eggs are represented by black, grey and white bars respectively (square root transformed data).

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5

30.0

a

20.0

10.0

0.0 19.3. 2.4. 16.4. 30.4. 14.5. 28.5. 11.6. 25.6. 9.7. 23.7. 6.8. 20.8. 3.9. 17.9.


5.0

b

4.0 3.0 2.0 1.0 0.0 19.3. 2.4. 16.4. 30.4. 14.5. 28.5. 11.6. 25.6. 9.7. 23.7. 6.8. 20.8. 3.9. 17.9.

5.0

c

4.0 3.0 2.0 1.0 0.0 19.3. 2.4. 16.4. 30.4. 14.5. 28.5. 11.6. 25.6. 9.7. 23.7. 6.8. 20.8. 3.9. 17.9.

FIGURE 3. Population development of T. urticae (= a), P. persimilis (= b) and N. californicus (= c) in greenhouse with release of P. persimilis + N. californicus. Adult, juveniles and eggs are represented by black, grey and white bars respectively (square root transformed data).

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The last application of insecticides and acaricides before the trial started was done two weeks before the first release of the predatory mites at the latest. The treatments included pyriproxifen against the whitefly Trialeurodes vaporariorum, mevinphos for aphid control and abamectin at half of the recommended field rate for spot treatment of spider mites. For the control of powdery mildew fungicide treatments were carried out at regular intervals during the whole growing season. Also during the trial period chemical treatment against aphids and thrips had to be applied (Table 1). All pesticides applied were chosen with regard to their harmless or only slightly harmful effect on both predatory mite species (Hassan et al. 1994; Oomen et al. 1991; Stolz 1994). Phytoseiulus persimilis and N. californicus originated from BIOHELP - Biological Systems (Vienna, Austria) and were released as mixed stage populations on Phaseolus vulgaris leaves either separately or in combination. The greenhouses were selected randomly with regard to the release strategy and the naturally occurring spider mite density, but were similar in size, number of plants and composition of rose varieties. Release rates and introduction intervals followed the recommendations of the advisory service (Table 1) at a rate of approximately 5 -10 predatory mites/ m2 every week or at appropriate intervals (Figures 1-3). The density of release sites differed from date to date with regard to the spider mite population development and the number of aggregations. Leaf samples were taken from the inner part and the lowest foliage layer present in a double row of rose plants. Spider mite infestations tend to build up first on these leaves and most of the spider mites occur on this part of the plants (Blümel 1990; Zhang & Sanderson 1995). The lower leaf canopy serves as shelter for the predatory mites because of the favourable climatic conditions. In addition, these leaves were not regularly removed at harvest. During the first eight weeks of the trial leaf samples were taken from approximately 50-60 cm above the ground (near the heating pipes) and later on, due to plant growth and the loss of older leaves, from about 90 – 100 cm above the ground. Fifty single leaves from a randomly stratified sample of the variety ”First Red” in each greenhouse were used to evaluate the population development of phytophagous and predatory mites. Mites were predominantly present on the lower surface of the leaves and to prevent their escape or damage collected leaves were placed upside down on moist filter paper. Numbers of all living developmental stages of spider mites and of both predatory mite species were counted under a stereomicroscope. A general problem for the interpretation of the control success was the lack of a well defined economic threshold for spider mite damage in greenhouse cut roses. In the present study supportive treatment with an acaricide was only done, when T. urticae had infested the upper part of the rose shoots, or when leaf damage was visible on these shoots. Control effect was judged as successful, when either no T. urticae infestation or feeding damage was visible on the rose shoots at harvest.

Results Climatic conditions Mean temperatures and relative humidities and their minimum-maximum ranges were similar in the three trial greenhouses. Mean temperatures varied in all greenhouses between 18°C and 27°C from the end of March until the middle of September. The minimum night temperature was 13°C and the maximum temperatures reached 42°C. The mean relative humidity ranged between 65% and 90%, with a minimum of 20% and a maximum of 100%. General distribution and development of mite populations Distributions both of spider mites and of predatory mites were observed to be highly aggregated, which resulted in large standard deviations of the mean mite densities, as described for T. urticae and 2002


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P. persimilis on roses and for T. urticae and N. californicus on strawberries (Sanderson & Zhang 1995; Greco et al. 1999). Spider mite populations developed a single infestation peak by the middle of June (Figures 1 and 2) in each of the two greenhouses where the predatory mite species had been released separately. In contrast, two infestation peaks of T. urticae were observed in the greenhouse with the mixed releases. The first peak occurred between the end of April and the middle of May and the second one at the end of July (Figure 3). The development of the predator populations frequently responded to the development of T. urticae with a temporal delay of approximately fourteen days (P. persimilis) or more (N. californicus). Releases of N. californicus alone Releases of N. californicus alone did not lead to a successful control of T. urticae without an additional treatment with a selective acaricide (Acorit 0.05%) (Figure 1). A spider mite density of 10.2 stages per leaf (0.3 SD 0.6 adults, 2.9 SD 12.4 juveniles and 7.1 SD 45.8 eggs per leaf sample; 69% mobile stages) was observed at the start of the trial, whereas N. californicus amounted to 0.2 stages per leaf (0 adults, 0.1 SD 0.6 juveniles and 0.1 SD 0.4 eggs per leaf sample; 67% mobile stages). At that date the prey: predator ratio was 57 T. urticae : 1 N. californicus. Until the middle of June the numbers of T. urticae per leaf increased constantly to a peak of 234.2 per leaf (42% mobile stages, 22.7 SD 24.3 adults, 75.0 SD 152.8 juveniles and 136.5 SD 229.6 eggs per leaf sample; Figure 1). At the same time the mean density of N. californicus, which had been released 7 times at a total amount of 33 mites/m², reached 5.2 stages per leaf (0.9 SD 1.9 adults, 1.7 SD 4.1 juveniles and 2.6 SD 8.1 eggs per leaf sample; Figure 1) resulting in a slightly improved prey : predator ratio of 45 : 1. The maximum density of 6.7 N. californicus per leaf (3.9 SD 3 adults, 0.8 SD 3.2 juveniles and 1.9 SD 5.2 eggs per leaf sample; 72% mobile stages) was reached at the end of June, two weeks after the peak infestation of T. urticae (Figure 1), which had declined to a mean density of 77.7 per leaf (9.2 SD 10.0 adults; 17.9 SD 39.7 juveniles; 50.5 SD 102.2 eggs per leaf sample; 34% mobile stages) at a shifted prey : predator ratio of 12 : 1. The spider mite infestation dropped below the threshold level (0.06 mites per leaf; prey : predator ratio 1 : 18) within six weeks after the peak infestation, when the release rate of N. californicus amounted 46 predators/m² in total and after two acaricide treatments had been applied. Subsequently the density of T. urticae remained at a negligible level until the end of the trial (Figure 1). After the reduction of the T. urticae population the density of N. californicus declined constantly to a low level (0.1 stages per leaf), but the phytoseiids persisted on the plants until the end of the trial (Figure 1). Neoseiulus californicus was also frequently observed on leaf samples, which were not infested with spider mites, but were partly inhabited with scales of T. vaporariorum. At the end of the trial the spider mite population (3.5 stages per leaf) as well as the mean density of N. californicus (0.6 stages per leaf) increased again, which resulted in a prey : predator ratio of 6 : 1. Although P. persimilis had not been released in this greenhouse, adult females occurred sporadically at the end of June and at the end of July, but did not establish (Figure 1). Releases of P. persimilis alone In the greenhouse with releases of P. persimilis alone the predatory mite was released four times (= 15 P. persimilis/m²) until the start of the peak infestation of T. urticae in the middle of June, but was not able to suppress the spider mite population. At the beginning of the trial a mean density of 0.4 T. urticae per leaf and very low numbers of P. persimilis were found, resulting in a prey : predator ratio of 19 : 1. Thus P. persimilis could not establish after two releases (9.6 mites/m² in total) during the first trial month. Consequently, the spider mite mean density increased until a maximum density of 178.8 T. urticae per leaf (29% 8


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mobile stages; 11.7 SD 17.8 adults stages; 39.3 SD 107.7 juvenile stages; 127.7 SD 390.7 eggs per leaf) at the end of June, despite three additional weekly releases of P. persimilis (19.6 mites/m²) and one acaricide treatment (Figure 2). At the same time the mean density of P. persimilis had reached a maximum of 2.2 mites per leaf (50% mobile stages; 0.7 SD 1.5 adults; 0.4 SD 1.2 juveniles; 1.1 SD 3.2 eggs). The prey : predator ratio had already started to decline from 339 : 1 in the middle of June to 83 : 1 at the end of June. Also concurrently N. californicus was found at a mean density of 1.5 mites per leaf, although it had not been released in this greenhouse. Mean numbers of N. californicus increased steadily from its first appearance six weeks after the trial start to a maximum of 2.5 N. californicus per leaf (0.4 SD 0.8 adults; 0.9 SD 3.0 juveniles; 1.2 SD 6.5 eggs; 53% mobile stages) at the beginning of July and thus exceeded the highest mean number of P. persimilis per leaf (ratio 2.7 N. californicus : 1 P. persimilis) (Figure 2). After three additional weekly releases of P. persimilis (14.4 mites/m²) from the end of June onwards, combined with one supportive acaricide treatment (Acorit 0.05%) the T. urticae infestation declined to a negligible level at the end of July until the trial was terminated. At the same time the numbers of both P. persimilis and N. californicus started to decline until they disappeared at the beginning of August (Figure 2). The spider mite population and both predatory mite populations increased again at the end of the trial (14.6 T. urticae, 0.02 P. persimilis and 0.06 N. californicus per leaf) resulting in a final prey : predator ratio of 181 : 1. Combined releases of N. californicus and P. persimilis In the greenhouse with combined, simultaneous release of both phytoseiid species the spider mite infestation was successfully controlled by 9 releases of the predatory mites (in total: 26 P. persimilis/m² + 24 N. californicus/m²) during the whole trial period without any supplementary chemical treatment. At the trial start the mean spider mite density amounted 23.9 stages per leaf (6.4 SD 12.8 adults, 9.5 SD 27.4 juveniles; 8.1 SD 21.9 eggs per leaf; 67% mobile stages), whereas the mean predatory mite densities were 0.8 per leaf (N. californicus) and 0.2 per leaf (P. persimilis) at a prey: predator ratio of 23 T. urticae : 1 phytoseiid (N. californicus + P. persimilis). The mean number of T. urticae per leaf increased to a first peak at the end of April with 73.1 spider mite stages per leaf (4.7 SD 8.4 adults; 16.9 SD 65.9 juveniles; 51.6 SD 196 eggs per leaf; 29% mobile stages)(Figure 3). At the same time the density of P. persimilis increased to 0.5 stages per leaf (0.1 SD 0.4 adults, 0.2 SD 0.9 juveniles, 0.2 SD 1.1 eggs per leaf; 52% mobile stages), whereas the density of N. californicus decreased to 0.4 per leaf (0.1 SD 0.3 adults, 0.1 SD 0.9 juveniles, 0.2 SD 1.4 eggs per leaf; 52% mobile stages), resulting in a prey : predator ratio of 80 : 1. The maximum densities of N. californicus and P. persimilis were recorded in the middle of May with 2.4 individuals per leaf for N. californicus (0.6 SD 1.0 adults; 0.5 SD 1.8 juveniles; 1.3 SD 3.3 eggs per leaf; 45 % mobile stages) and 2.5 individuals per leaf for P. persimilis (0.8 SD 1.3 adults; 1.0 SD. 2.6 juveniles; 0.7 SD 2.1 eggs; 73% mobile stages)(Figure 3). Concurrently, a decrease of the spider mite density (52.6 per leaf) and a shift in the prey : predator ratio to 10 : 1 was observed. From the start of June until the middle of July the T. urticae infestation collapsed, but reappeared and developed a second peak infestation at the end of July with 25.7 stages per leaf (1.4 SD 2.9 adults; 8.4 SD 46.6 juveniles; 15.9 SD 63.3 eggs per leaf; 38% mobile stages), which declined to a negligible level (0.6 T. urticae per leaf) four weeks later (Figure 3). The mean numbers of P. persimilis increased and decreased parallel to the spider mite population development, whereas the density of N. californicus increased at the mid of August (0.4 per leaf) and remained at a high level (0.2 per leaf) until the end of the trial. The prey : predator ratio changed from 10 : 1 in the middle of August to 1.5 : 1 at the end of the trial. During this period also the ratio N. californicus : P. persimilis

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shifted from a ratio 1 : 1 or a P. persimilis biased ratio to a N. californicus biased ratio at the end of the trial (5 : 1).

Discussion The study results are discussed separately for each greenhouse, as a direct comparison of the effect of the three release strategies on spider mite control is impeded by several factors: i) naturally occurring T. urticae densities at the start of trial differed among the greenhouses, ii) release rates of predatory mites were not comparable, and resulting from i) and ii) prey : predator ratios were not comparable, iii) release strategies were not replicated iiii) differences in the susceptibility of the two phytoseiid species towards the applied plant protection products (Croft et al. 1976; Blümel 1999). Under the present study conditions and given prey : predator ratios, neither N. californicus nor P. persimilis could sufficiently suppress the T. urticae infestation when released separately either once or repeatedly. The strategy to release N. californicus alone was not successful in controlling the naturally occurring T. urticae infestation on the roses in this study. The high spider mite density at the start of the trial resulting in a prey : predator ratio of 57 : 1 was unfavourable for a rapid reduction of the T. urticae population by N. californicus. This is probably due to its nature as generalist predator, which does not exhibit an equally strong numerical and functional response towards spider mites as a prey specialist (Friese & Gilstrap 1982; Gilstrap & Friese 1985; Croft et al. 1998). Although the short-term control of the spider mite infestation could only be achieved by repeated releases of N. californicus combined with two supplementary treatments with selective acaricides, the successive long-term suppression below the threshold until the end of the season was probably caused by N. californicus. This is especially supported by the shift of the prey : predator ratio from a prey biased ratio to a predator biased ratio of 1 : 18 at the end of July , which was still maintained at 1:7 at the middle of August. The phytoseiid was constantly present on the plants until the termination of the evaluation period, despite the spider mite density was negligible. Neoseiulus californicus was even found on leaves without any spider mites but infested with whitefly scales, which could have served as food source, both directly through host feeding and indirectly as a source of honeydew (Nomikou et al. 2001; Blümel personal observation). These findings are consistent with the classification of N. californicus as generalist predator, which is favourable for the formation of long term populations even at low or diminishing prey densities of tetranychid prey, due to its overall broad food range (Swirskii et al. 1970; Castagnoli & Falchini 1993; Croft et al. 1998). Phytoseiulus persimilis, which invaded from other greenhouses and/or was accidentally introduced by workers could not establish in the N. californicus greenhouse despite an increasing T. urticae density. Only adult females were found sporadically and disappeared again within four weeks after its first appearance at the end of June. The population development of P. persimilis could have been impeded by both the low prey level, which lead to a reduced number of offspring, and the simultaneous presence of N. californicus, which may have resulted in intraguild predation and displacement of the specialist P. persimilis (Walzer and Schausberger 1999 a, b). The long-term persistence of N. californicus could not completely suppress the recovery of the T. urticae population at the end of the trial. However, the spider mite numbers increased to a low density at a prey : predator ratio of 6 :1, which should allow a sufficient predator density for the start of the next growing season, as N. californicus can diapause and overwinter in the greenhouse. The introductions of P. persimilis alone could not sufficiently suppress T. urticae in this study. Probably the low density of T. urticae at the start of the trial (prey : predator ratio of 19 : 1), did not provide sufficient prey for a population build-up of the phytoseiid, which is specialised on web 10


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producing tetranychids (Kennett & Hamai 1980; Sabelis 1985; McMurtry & Croft 1997). Additionally, the presence of P. persimilis could have been affected by intraspecific competition, which may accelerate the population decrease of P. persimilis in times of food scarcity (Schausberger & Walzer 2001). However, intraguild predation by N. californicus is considered as the main reason for the population decline of P. persimilis. After an accidental invasion N. californicus became established earlier in the season than P. persimilis (at the end of May the ratio was 1.6 N. californicus : 1 P. persimilis) and was present on the plants after the spider mite population had declined for a longer period than P. persimilis (final ratio 3 N. californicus : 1 P. persimilis). Even at a strong increase of the T. urticae density during the season, resulting in a prey : predator ratio of 339 : 1, the mean P. persimilis numbers rose to only a limited extent ( 2.2 mites per leaf). These observations indicate the problems of synchronisation of mixed releases of two phytoseiid species with different life styles, as the prey specialist population could be affected by the low T. urticae density and/or a high density of the generalist N. californicus (Schausberger & Walzer, 2001). A recovery of the spider mite population occurred after four weeks of disappearance, leading to a prey : predator ratio of 181 : 1 at the end of the trial, which is unfavourable for suppressing the spider mite population in the following season. Successful long-term control of spider mite infestation in greenhouse roses by repeated releases of P. persimilis has been reported only once (Gough 1991), however, without noting the presence of other phytoseiid species or other biological control agents, which could have interfered with P. persimilis. In addition, the persistent control effect described by Gough (1991) could have been due to the constant invasion of prey mites from outdoor crops and weeds. In this study where both phytoseiid species were released simultaneously, T. urticae was controlled effectively throughout the season, even though the infestation level of T. urticae was relatively high at the onset of the trial. However, the damage threshold was rarely exceeded, as the prey : predator ratio at the two spider mite infestation peaks amounted 80 and 42 T. urticae to 1 phytoseiid (N. californicus + P. persimilis) and declined to 2 T. urticae to 1 phytoseiid at the end of the trial. The predator : predator ratio shifted several times from N. californicus to P. persimilis and vice versa and was strongly biased towards N. californicus at the termination of the trial. Both, the final prey : predator ratio and the final predator : predator ratio form a favourable starting point for the early suppression of spider mite populations in the following growing season. The combined release of both predatory mite species was done to detect whether phytoseiids with different predation types were complementary or gave more successful control of T. urticae than releases of each phytoseiid species separately (Croft & MacRae 1992 a,b). An additive or synergistic control resulting in sustainable and long-term pest control could prove economically advantageous for semi-persistent greenhouse crops, such as cut roses, which are mainly produced the whole year round. Despite photoperiod and temperature conditions during the winter period in greenhouses in temperate climatic zones, not all individuals of a T. urticae population enter diapause and new infestations can build up rapidly early in the next growing season (van de Vrie 1985). This underlines the need for predatory mites to be present in the greenhouse either throughout the whole growing season or as early as possible at the start of the growing season. Although a direct comparison of the three different release strategies with regard to the control of T. urticae was not possible in this study, it was shown, that even at a high starting infestation level of T. urticae, the combined, simultaneous release of both predatory mite species resulted in successful long term control. Phytoseiulus persimilis responded almost immediately to fluctuations in the population of T. urticae, whereas N. californicus increased in response to the population increase of both other mite species. In addition N. californicus was found on leaves that did not harbour spider mites in all greenhouses.

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The fact that N. californicus persisted longer and was more abundant than P. persimilis and that N. californicus had possibly displaced P. persimilis, indicates that the release strategies for a combined use of these two predators could be optimised towards a sequential introduction strategy. However, sequential releases of both phytoseiid species should be well synchronised, as otherwise either a low prey density for the diet specialist or a high density of the generalist could affect the specialist population and thus endanger the control effect (Schausberger & Walzer 2001). It remains to be studied, whether an early season establishment of N. californicus populations, complemented by additional releases of P. persimilis in high density patches of T. urticae at regular intervals, will improve the biological control efficacy of T. urticae in greenhouse roses.

Acknowledgements We gratefully acknowledge the critical review of the manuscript and the helpful comments by P. Schausberger, Institute of Plant Protection, University of Agricultural Science, Vienna, and by A. M. de Courcy-Williams, HRI, UK. We are also very grateful for the technical assistance of H. Hausdorf, BFL, Institute of Phytomedicine, Department of Biological Plant Protection and Horticulture.

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