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Biological and Microbial Control

Compatibility of Bifenazate and Phytoseiulus persimilis for Management of Twospotted Spider Mites in North Carolina Staked TomatoesTom R. Bilbo and James F. Walgenbach1

Department of Entomology and Plant Pathology, Mountain Horticultural Crops Research and Education Center, North Carolina State University, 455 Research Drive, Mills River, NC 28759 and 1Corresponding author, e-mail: jim_walgenbach@ncsu.edu

Subject Editor: Cheryle O'Donnell

Received 29 April 2020; Editorial decision 30 June 2020

Abstract

The twospotted spider mite (TSSM, Tetranychus urticae Koch) is a key pest of tomatoes (Solanum lycopersicon L. [Solanales: Solanaceae]) in North Carolina, and its management has relied principally on synthetic acari-cides. Augmentative biological control of TSSM is a commonplace and effective management strategy in greenhouses worldwide, but in field-grown vegetable crops biocontrol of TSSM is poorly developed. We con-ducted small-plot field experiments in 2016 and 2019 to test the ability of the predatory mite, Phytoseiulus persimilis Athias-Henriot, to establish, disperse, and reduce TSSM in staked tomatoes, as well as test their compatibility with a commonly used reduced-risk acaricide, bifenazate (Acramite). Across both years, the most effective treatment for reducing TSSM was the combination of P. persimilis + Acramite. Phytoseiulus persimilis successfully established both years, but its population growth and dispersal were greater in 2016 than 2019. Acramite alone significantly reduced TSSM pressure in 2019 and P. persimilis alone did not reduce TSSM pres-sure below the control in either year. However, results in 2016 were influenced by the eventual dispersal of P. persimilis into all experimental plots, despite efforts to hinder their movement with corn barriers. Results in 2019 were influenced by the late-season invasion of TSSM into the trial, which delayed P. persimilis releases and influenced their establishment and growth. This study is the first to demonstrate the utility and limitations of P. persimilis in staked field tomatoes, which is a promising option for growers to manage TSSM in tomatoes in the southeast United States.

Key words: twospotted spider mite, Phytoseiulus persimilis, bifenazate, tomato, biological control

The twospotted spider mite (TSSM, Tetranychus urticae Koch, Acari: Tetranychidae) is a serious pest of tomatoes (Solanum lycopersicon L. [Solanales: Solanaceae]) in many parts of the world. In western and central North Carolina, it consistently reaches pest status and without management its feeding can reduce fruit production and de-crease marketable quality of fruit, including cosmetic damage known as gold fleck (Meck et  al. 2012, 2013). The traditional approach to managing TSSM in tomatoes is through multiple applications of acaricides, but this reliance on chemical control has a number of limitations and drawbacks, including high costs, resistance develop-ment, and harvesting limitations.

Relative to other commonly used pesticides in tomatoes, acari-cides that are effective against TSSM can be very expensive, ex-ceeding $120/ha (Meck 2010). The high fecundity rate and short life cycle of TSSM contributes to rapid population buildup, especially

under hot, dry climatic conditions (Brandenburg and Kennedy 1987, White and Liburd 2005), the former also facilitating the rapid de-velopment of resistance to pesticides (van Leeuwen et  al. 2010). In North Carolina, TSSM populations typically increase rapidly in July and August, which coincides with the beginning of tomato harvest and puts fruit at risk of direct feeding injury and unmar-ketable cosmetic damage. Because of the labor-intensive nature of tomato production, especially during harvest, reentry intervals can often restrict or limit the use of pesticides, including acaricides. This contributes to growers applying acaricides prophylactically ahead of harvest, regardless of the density of TSSM populations. The appli-cation of acaricides/insecticides also poses risks to the environment and nontarget organisms, as well as added costs associated with using heavy spray equipment, such as soil compaction, gasoline, and general wear and tear on equipment (Ghidiu et al. 2012).

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Biological control of TSSM has been commonplace in green-houses since the 1960s (McMurtry and Croft 1997), but in field vegetables it has been less studied and underutilized. A number of predatory mites prey on TSSM, but the most effective is the spe-cialist predator, Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) (McMurtry and Croft 1997). This predator locates TSSM using volatile chemicals emitted by attacked plants, and in the absence of prey they will disperse from a field in search of food (De Boer et al. 2004). Phytoseiulus persimilis adults feed on all life stages of TSSM, while nymphs feed only on eggs, larvae, and protonymphs (Takafuji and Chant 1976). They disperse and move among plants either by walking or aerially, and these behaviors are influenced by a number of factors, including prey density, predator hunger, wind speed, temperature, humidity, and plant height (Jung and Croft 2001a, b).

Phytoseiulus persimilis is a highly voracious and effective predator of TSSM on a number of plant species and, when applied correctly under the right environmental conditions, can provide ex-cellent and long-lasting management of TSSM. In California and Florida, P.  persimilis has been used successfully to manage TSSM in field-grown strawberries (Oatman et  al. 1968, Decou 1994, McMurtry and Croft 1997, Rhodes and Liburd 2006), but the use of predators in tomatoes has been more challenging. The efficacy of P. persimilis in tomatoes and other solanaceous crops is thought to be limited because of the physical and chemical deterrents produced by trichomes (Simmons and Gurr 2005), but there is evidence that P. persimilis can adapt to tomato plants after rearing for several gen-erations on TSSM infested tomato plants (Drukker et al. 1997).

Another challenge to the success of P.  persimilis in vegetable cropping systems is the relative toxicity of the numerous pesticides typically applied to fruiting vegetables (Southeastern US Vegetable Crop Handbook 2020). Several studies have investigated the sensi-tivity of P. persimilis and other predatory mites to commonly used pesticides and have found a wide range of toxicity (Ditillo et  al. 2016, Bergeron and Schmidt-Jeffris 2020). Acramite (bifenazate) is a reduced-risk acaricide that is highly effective against TSSM, but has shown to have relatively low toxicity to predatory mites (Rhodes and Liburd 2006, Liburd et al. 2007). Rhodes and Liburd (2006) evaluated the compatibility of P.  persimilis and Acramite in field-grown strawberries and demonstrated that their combined use was an effective strategy for reducing TSSM populations. But it is un-known if similar results are to be seen in tomatoes given the differ-ences in crop management, seasonality, and host plant effects such as glandular and nonglandular trichomes of tomato (Simmons and Gurr 2005, Rojas et al. 2013, Ditillo et al. 2016).

The objective of this study was to evaluate the efficacy of P. persimilis to reduce TSSM in staked tomatoes, test their compati-bility with a commonly used reduced-risk acaricide (bifenazate), and observe predatory mite movement through tomatoes from a single release point. To our knowledge, this is the first study to demon-strate the use of P. persimilis for TSSM management in field-grown tomatoes.

Materials and Methods

We conducted a 2-yr study at the North Carolina State University Mountain Horticultural Crops Research Station in Mills River, NC, to determine the efficacy and compatibility of biological and chemical control for suppression of twospotted spider mite (TSSM, T.  urticae) in staked field tomatoes. We conducted a single, aug-mentative release of the predatory mite P.  persimilis at a rate of

approximately 20,000 predatory mites per acre. This rate is based on results from previous field experiments (unpublished data). In 2016, P. persimilis, originally collected from a commercial tomato field in Rowan County, NC, were reared on TSSM-infested tomato plants in a greenhouse prior to release in research plots. In 2019, P. persimilis were obtained from Koppert Biological Systems (Spidex, Berkel en Rodenrijs, The Netherlands) and released into the field within 24 h of receiving the shipment. The chemical control agent was a single foliar application of the reduced-risk acaricide bifenazate (Acramite 50WP, formerly Chemtura Corporation, now Banter 50WDG, UPL, King of Prussia, PA). Acramite was applied at a rate of 0.56 kg a.i./ha and sprayed with a CO2-powered backpack sprayer delivering 580 liters/ha through four hollow cone nozzles per row at 275 Kpa (each row was sprayed with a 2-nozzle wand on each side of the row). Treatments consisted of a single application of Acramite, a single release of P. persimilis, a combination of Acramite plus P. persimilis, and a nontreated control. Acramite applications were made when TSSM counts in the two Acramite treatments (with and without P.  persimilis release) first exceeded a threshold of eight mites per leaflet (Meck et al. 2013). Treatments were arranged in a 4 × 4 Latin Square with four replicates for each treatment.

In 2016, 5-wk old tomato (Solanum lycopersicum L. ‘Monticello’) transplants were planted on 15 June into black plastic mulched beds with drip irrigation and managed with standard practices such as pruning, staking, stringing, fertilization, weed management, and a standard fungicide program (Kemble et al. 2019). Fungicides were applied weekly at labeled rates and included one or more of the following: acibenzolar-S-methyl (Actigard), boscalid (Endura), chorothalonil (Bravo), mancozeb, copper, difenoconazol + cyprodinil (Inspire Super), penthiopyrad (Fontelis), and azoxystrobin (Quadris). Each treatment consisted of small plots of five rows that were each 7.6 m long. Plants were spaced 0.46 m apart within rows and row centers were spaced 1.5 m apart. Replicates were separated by 7.6 m alleys with field corn (Zea mays) planted in between plots and replicates to hinder the movement of P. persimilis between plots. Sampling for mites was conducted from 19 July through 12 September. Phytoseiulus persimilis were released on 25 July when TSSM populations across all treatments averaged 0.55 TSSM per leaflet. Approximately 300 P. persimilis were released into the center of each 58 m2 plot for the treatments testing P. persimilis alone or in conjunction with Acramite sprays. P. persimilis were introduced to plots by sprinkling mites from the provided mite and vermiculite product onto a white sheet of paper (to count and observe survival and activity) and then shaken onto the top one-third of the plant canopy.

Sampling for both TSSM and P. persimilis was conducted in situ by sampling five random leaflets—terminal leaflets of the second or third most recently expanded leaf—from each row and counting the number of motile TSSM (nymphs and adults visible with 10× visor lens) and nymphs and adults of P. persimilis. Acramite was sprayed on 15 August when TSSM populations averaged 21.1 mites per leaflet across all non-P. persimilis plots.

In 2019, 5-wk-old tomato transplants (‘Mountain Majesty,’ as ‘Monticello’ were unavailable from local dealers in 2019) were set on 13 June and managed similarly as above. Each treatment con-sisted of small plots of three rows (plot size reduced from 2016 due to space constraints) that were each 7.6 m long. Field design was the same as above except that soybeans (Glycine max) were planted between plots and replicates to limit P. persimilis movement. Plot borders were switched from corn in 2016 to soybean in 2019 to avoid problems encountered when driving sprayers through corn to apply fungicide in 2016. Sampling was conducted from 4 July through 24 October, and sampling within individual rows began on

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25 July. Phytoseiulus persimilis were released on 6 September when TSSM populations across all treatments averaged 0.68 TSSM per leaflet. Approximately 200 P. persimilis were released into the center of each 34.8 m2 plot for the treatments testing P. persimilis alone or in conjunction with Acramite sprays. Mites were sampled same as above and Acramite was sprayed on 27 September when TSSM populations averaged 9.2 mites per leaflet across all non-P. persimilis plots. On 27 September and 10 October flonicamid (Beleaf 50SG, FMC Corp. Philadelphia, PA) and acetamiprid (Assail 30SG, UPL, King of Prussia, PA), respectively, were sprayed to suppress potato aphids (Macrosiphum euphorbiae Thomas). These compounds have little to no toxicity against either TSSM or P. persimilis (Ditillo et al. 2016, Bilbo and Walgenbach 2020).

Data AnalysesTo compare the pest and predator pressure within each treatment, season total cumulative mite days (CMD) were calculated by multi-plying the average mite density on successive sample dates by the sampling interval (days), and summing all mite days over all sam-pling dates (Ruppel 1983). CMD is a useful metric of pest density over time and tends to correlate with fruit yield and cosmetic damage, such as in tomato (Meck et  al. 2012, 2013), strawberry (Walsh et al. 1998, Nyoike and Liburd 2013), and cucumber (Park and Lee 2005). CMD among treatments for TSSM and P. persimilis were analyzed separately using a one-way analysis of variance (ANOVA; PROC MIXED, SAS Institute 2018) with CMD as the fixed effect and replication as a random effect.

The dispersion of P. persimilis among rows within each plot was analyzed for the P.  persimilis release only treatment to determine the extent of P. persimilis movement and TSSM suppression in rows away from the release row. Center rows (where P. persimilis were released) were compared with the average of either rows 2 + 4 and 1 + 5 in 2016, or rows 1 + 3 in 2019. Linear mixed repeated meas-ures models (PROC MIXED, SAS Institute 2018) were constructed

for TSSM and P. persimilis each year with number of mites per five leaflets as the dependent variable and row, week, and their inter-action as fixed effects. Replication was used as a random effect. The denominator degrees of freedom were calculated following the methods of Kenward and Roger (1997). Variance–covariance struc-ture was specified as compound symmetry based on lowest AICc value (Hurvich and Tsai 1989). When interactions were significant, the SLICE function (PROC MIXED) was used to identify differences between rows within each sampling week. In all analyses, means were separated using Tukey’s HSD when significant at α < 0.05 (Tukey 1953). Residual plots (residual by predicted values) were visually inspected for deviations in normality and constant variance and season CMD and number of mites were log10(x+1)-transformed to improve model assumptions.

Results

Establishment and Population Dynamics of Twospotted Spider Mites and P. persimilisIn both 2016 and 2019, TSSM naturally infested the experimental trials and their populations increased beyond the economic injury level of eight mites per leaflet (Meck 2010, Meck et al. 2013) in all plots. The timing of field invasion and extent of population increase differed among years.

In 2016, when sampling began on 19 July, TSSM populations averaged 0.24  ± 0.08 (SEM) mites per leaflet across all plots. Populations in all treatments increased steadily until peaking on 15 August and were highest in the two treatments where P. persimilis had not previously been released: 24.5 ± 9.0 and 17.7 ± 7.0 mites/leaflet in the Acramite and control treatments, respectively (Fig. 1). The following week TSSM decreased in all treatments except the control, where the population remained at 17.4 ± 3.9 mites/leaflet, but then began decreasing the following week due to invasion of P. persimilis into the control plots (discussed subsequently).

Fig. 1. Population dynamics of twospotted spider mites (TSSM) and P. persimilis in small plots of staked tomatoes in Mills River, NC in 2016. Mean (± SEM) number of mites were recorded weekly. Open arrow indicates timing of P. persimilis release into plots. Closed arrow indicates timing of Acramite application.

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In 2016, P.  persimilis successfully established in both re-lease treatments and populations increased rapidly 3  wk after their release (Fig.  1). Phytoseiulus persimilis invaded both the Acramite-only treatment and the control despite efforts to hinder their movement between plots. In the control treatment, P.  persimilis were detected at low levels on 22 August, 1  wk after their numbers spiked in the P. persimilis-only plot. Their overall population-dynamics in the control mirrored that of the P. persimilis-only treatment but with a 1-wk lag. The high P. persimilis numbers in the P. persimilis and control treatments, and the low P.  persimilis numbers in both Acramite-sprayed treatments, indicates that P. persimilis readily dispersed into all plots, but that the application of Acramite resulted in signifi-cantly fewer P. persimilis.

In 2019, natural TSSM infestations arrived much later in the season and were slow to build. A single TSSM was first detected on 2 August and populations across all treatments remained below 3.5 mites/leaflet until 26 September (Fig.  2). Between September 19 and 26 TSSM populations increased rapidly and similarly across all treatments to 9.6 ± 1.1 mites/leaflet. After this date, TSSM populations generally continued to increase in the treatments not sprayed with Acramite, and the Acramite-sprayed treatments increased steadily after an initial knock-down from the Acramite application. Across all treatments, TSSM popula-tions appeared to increase or stabilize until sampling was termin-ated when a frost killed the tomato plants.

In 2019, P.  persimilis successfully established and increased in both release treatments, with an apparent population increase 4 wk after release (Fig. 2). Phytoseiulus persimilis numbers in 2019 were far lower and temporally delayed compared with in 2016, likely due to being released later in the season when temperatures were cooler. Phytoseiulus persimilis were detected in both the Acramite-only treatment and the control, but never noticeably increased prior to the termination of sampling.

Phytoseiulus persimilis Dispersal from Release PointThe natural dispersal of P.  persimilis among rows within a plot was analyzed only for the P.  persimilis release-only treatment (Table 1). Dispersion was not analyzed for the treatment combining P. persimilis and Acramite, as Acramite appeared to have a signifi-cant influence on P.  persimilis populations (discussed earlier). In 2016, differences in P. persimilis numbers by row became apparent 3  wk after their release. Phytoseiulus persimilis significantly in-creased in the center row and rows 2 + 4 (adjacent to center row), but remained low in the outer rows (rows 1  +  5). The following 2 wk, P. persimilis decreased in the center row and rows 2 + 4, while increasing and becoming significantly higher in rows 1 + 5 (Fig. 3). The 1-wk delay in P. persimilis growth in the outermost rows (1 + 5) was reflected by less overall TSSM suppression in the outermost rows, and to a lesser extent, rows 2 + 4 (Fig. 3). By 6 September, 6  wk after P.  persimilis were released, P.  persimilis were virtually absent from all P. persimilis-only plots. Overall, TSSM populations were significantly lower in the center row than in rows 2 + 4 and 1 + 5 (Table 1).

In 2019, plots consisted of three rows each, and P.  persimilis were released on 6 September. They were first detected 4 wk later on 3 October in the center row and numbers increased steadily and peaked on the final sampling date at a density of 4.3 ± 2.0 mites/ five leaflets. In the outer rows (rows 1 + 3), P. persimilis were not detected until 17 October, never exceeded 0.5 mites/ five leaflets, and were significantly less abundant than in the center row for the final three sampling weeks (Fig. 3). Phytoseiulus persimilis numbers in 2019 were far fewer and temporally delayed compared with in 2016, likely due to being released later in the season when temper-atures were cooler. The failure of P. persimilis abundance to increase quickly or large enough resulted in the failure to decrease TSSM populations in any of the rows. TSSM increased and stayed high until sampling was terminated due to freezing temperatures (Fig. 3).

Fig. 2. Population dynamics of twospotted spider mites (TSSM) and P. persimilis in small plots of staked tomatoes in Mills River, NC in 2019. Mean (± SEM) number of mites were recorded weekly. Open arrow indicates timing of P. persimilis release into plots. Closed arrow indicates timing of Acramite application.

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Efficacy of P. persimilis and Acramite for TSSM SuppressionThe overall efficacy of P.  persimilis and/or Acramite to sup-press TSSM populations was analyzed using season total CMD. In 2016, P.  persimilis CMD were significantly higher in both the P.  persimilis-only treatment and the control treatment rela-tive to both of the Acramite-treated plots (Fig. 4). Average TSSM CMD was significantly lower in the combination treatment, P.  persimilis and Acramite, compared with the control (Fig.  4). Since P. persimilis CMD in the control was equal to in the release treatment, this likely influenced differences in TSSM CMD across treatments.

In 2019, P. persimilis were more restricted to their release treat-ments, with virtually no CMD recorded in either the Acramite or control treatment (Fig.  4). Phytoseiulus persimilis CMD were significantly higher only in the P.  persimilis-only treatment. TSSM CMD were significantly reduced in both the Acramite and Acramite + P.  persimilis treatments, with no noticeable effect of P. persimilis alone.

In both 2016 and 2019, Acramite was very effective at reducing motile TSSM populations. In 2016, in the Acramite treatment, TSSM populations were reduced by 98.8%, from 24.5 to 0.3 mites/leaflet by 7 d after treatment (Fig. 1). However, because Acramite was not sprayed until TSSM populations averaged 24.5  ± 9.0 mites/leaflet

Table 1. ANOVA results for number of twospotted spider mites (TSSM) and P. persimilis among rows within small plots of staked tomatoes. Mills River, NC, 2016 and 2019

Year Mite Factor

Number of mites

df F P

2016 TSSM Row 2, 9 7.8 0.011 Week 8, 72 47.1 <0.001 Row × Week 16, 72 1.1 0.354 P. persimilis Row 2, 6 0.6 0.573 Week 8, 72 51.4 <0.001 Row × Week 16, 72 9.2 <0.001

2019 TSSM Row 1, 2.86 1.5 0.315 Week 13, 75.9 81.6 <0.001 Row × Week 13, 76 0.7 0.764 P. persimilis Row 1, 3.05 10.37 0.048 Week 13, 76.2 6.95 <0.001 Row × Week 13, 76.2 3.83 <0.001

Fig. 3. Dispersal of P. persimilis and infestation of twospotted spider mite (TSSM) by plot row in small plots of staked tomatoes in Mills River, NC in 2016 and 2019. Mean (± SEM) number of mites were recorded weekly. Plots consisted of five rows and three rows in 2016 and 2019, respectively. Open arrow indicates timing of P.  persimilis release into plots. Asterisk (*) indicates where SLICE function was used to identify significant differences among rows within each sampling week when the week × row interaction was significant.

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(TSSM density in the Acramite-only treatment), there was enough TSSM pressure (CMD) that final differences were not apparent (Fig. 4). In 2019, in the Acramite treatment, TSSM populations were reduced 76.4% the week following the acaricide spray, although the effect was short-lived and TSSM populations continued to increase in the remaining two sampling weeks (Fig. 2). In 2019, the reduced development of motile P. persimilis populations and their impact on TSSM CMD was likely a result of the cooler temperatures in late-September and October. The trial was terminated on 24 October at the onset of freezing temperatures.

Discussion

Biological control of agricultural arthropod pests is an important component of integrated pest management because it can improve pest suppression and reduce economic and environmental costs (Bale et al. 2008). Often, though, biological control is not a stand-alone solution and needs to be incorporated into a larger pest management context, which frequently includes the application of chemical pesti-cides. We conducted a 2-yr study in western North Carolina to inves-tigate the use of the predatory mite P. persimilis and the reduced-risk acaricide Acramite for the management of twospotted spider mites in staked tomatoes. Our study demonstrated the compatibility of Acramite and P. persimilis for suppression of TSSM, and shed light on the important factors for successfully releasing and establishing P. persimilis in staked tomatoes.

TSSM is a consistent pest of tomato in western and central NC, but the timing of infestation can be variable, which in turn can in-fluence the potential for biological control. Phytoseiulus persimilis is an obligate specialist predator of spider mites and in their ab-sence they will readily disperse (De Boer et  al. 2004). Therefore,

P.  persimilis should not be augmentatively introduced into a field until spider mites have established. In 2016, TSSM infested tomatoes by late July and increased significantly throughout August, when average daily temperatures averaged 23.2°C. Under these condi-tions, released P. persimilis populations in our study increased and readily dispersed from singular release points into surrounding rows and all surrounding plots (Figs. 1 and 3), despite efforts to hinder their movement with corn borders. In contrast, TSSM populations in 2019 did not infest the trial until mid-August and did not sig-nificantly increase until mid-September (Fig. 2). The delay in TSSM establishment delayed the release of P. persimilis, which appeared to influence their growth and dispersal. Phytoseiulus persimilis in-creased significantly only in the center row where it was released, but this growth was far less than in 2016 and did not result in any noticeable reduction in TSSM populations (Fig. 1).

Our results demonstrate that under optimal environmental con-ditions (as in 2016), P.  persimilis populations build to detectable levels approximately 3  wk after their release, and reduce TSSM populations by the fourth week postrelease. These results coin-cide with numerous other P. persimilis releases we have conducted in commercial tomato fields throughout western and central NC (unpublished data). In contrast, P. persimilis in 2019 were not de-tected until 4 wk postrelease, and numbers remained low relative to 2016. Contributing factors to lower P. persimilis populations in 2019 versus 2016 were likely the delayed and lower TSSM popula-tions in 2019, and also lower temperatures during the month after P. persimilis releases (23.2 vs 19.8°C in 2016 and 2019, respectively).

Another possible factor influencing P. persimilis effectiveness and growth is the host plant it is adapted to prior to release. In 2016, P. persimilis released in this study were collected and reared on to-mato prior to release. In 2019, P. persimilis were obtained from a

Fig. 4. Mean (± SEM) cumulative mite days (CMD) of twospotted spider mites (TSSM) or P. persimilis in small plots of staked tomatoes in Mills River, NC in 2016 and 2019. P. persimilis were released and Acramite was applied only once. Bars with the same letter were not significantly different at α = 0.05 (Tukey’s HSD test).

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commercial insectary (Koppert Biological Systems), where they are typically mass-reared on spider mite-infested bean plants (Phaseolus vulgaris L.). Drukker et al. (1997) reported that when P. persimilis were mass-reared on tomato for four generations before release on greenhouse tomatoes, they had improved growth and spider mite control compared with an identical bean-adapted strain. Differences among strains may have been an important factor in this study influencing the performance of P.  persimilis. We have ongoing re-search trials to determine whether the source of P.  persimilis sig-nificantly influences its performance on staked tomatoes under field conditions.

In this study, the only treatment to reliably reduce TSSM pressure below the control in both years was the combination of Acramite and P. persimilis (Fig. 4). Phytoseiulus persimilis alone did not sig-nificantly reduce TSSM pressure either year, and Acramite alone provided significant control only in 2019. It is important to note, however, that differences in 2016 would likely have been more pronounced had P.  persimilis not invaded control plots, where it mostly eliminated TSSM by 6 September (1  wk later than in the P.  persimilis release plots). The switch from corn to soybean plot borders in 2019 appeared to be a more effective barrier in preventing P. persimilis movement between plots. This could have been due to a more dense plant canopy or differences in plant height that af-fected aerial dispersal. In 2016, the Acramite application was very effective at reducing TSSM populations but was applied later than normally recommended and TSSM pressure had already significantly accumulated. TSSM populations never rebounded, but it is uncertain if this was due solely to the Acramite application since P. persimilis had also invaded these plots and were present at low levels during and after the Acramite application. In an experiment in strawberries, Rhodes and Liburd (2006) intentionally delayed an application of Acramite until TSSM numbers were very high, and found that Acramite could not significantly reduce TSSM levels at that point. These data demonstrate the importance of timing Acramite appli-cations before TSSM populations get too high. However, our results suggest that if P. persimilis is present, late-applied Acramite may still be highly efficacious.

Our results support the conclusion that others have made that Acramite can be used concurrently with P. persimilis for managing spider mites (Rhodes and Liburd 2006, Rhodes et al. 2006). While Acramite + P.  persimilis provided the best and most consistent control overall, Acramite did influence P.  persimilis populations compared with the P. persimilis-only treatment (Figs. 1, 2 and 4). However, it could not be determined in our study whether this was due to toxicity or to changes in the P. persimilis food source (TSSM), thus influencing P. persimilis behavior. A number of studies have re-ported the relatively low toxicity of Acramite to P. persimilis in both greenhouse and laboratory studies (Liburd et  al. 2007, Bergeron and Schmidt-Jeffris 2020). It would be valuable for future studies to determine the compatibility between P. persimilis and Agri-Mek (Abamectin; Syngenta Crop Protection, Inc., Greensboro, NC) in staked tomatoes, as this is another highly effective and commonly used acaricide in North Carolina, but is rated as slightly more toxic to P. persimilis than Acramite (Bergeron and Schmidt-Jeffris 2020).

Overall, our study revealed that P. persimilis and Acramite are two compatible control methods and together provide effective and lasting suppression of TSSM. Despite the perceived impediments of using P. persimilis in tomatoes due to host plant characteristics, we demonstrated that P. persimilis can readily establish and disperse in staked tomatoes under the right environmental conditions. Ongoing and future studies will better resolve the most effective way to intro-duce and protect P.  persimilis in staked tomatoes. These include

various banker plant systems, conservation of naturalized popula-tions that occur in central North Carolina (Ditillo et al. 2016), and how to best time Acramite applications and P.  persimilis releases. As research efforts continue more management tactics will become available to growers, which will reduce their reliance on chemical control while incurring the added benefits of improved pest man-agement, increased profits, greater harvesting flexibility, and better environmental conservation.

Acknowledgments

We thank Steve Schoof, Lindsey Stump, Amelia Heintz-Botz, Taylor Ackley, Alex Lines, and Cooper Dalton for technical assistance. This study was funded, in part by USDA-NIFA Southern Region SARE project LS17-284, and the NC Agricultural Research Service.

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