Efficacy of natural enemies against the tobacco thrips Thrips parvispinus (Karny) in laboratory and greenhouse studies

Abstract

BACKGROUND

The tobacco thrips, Thrips parvispinus, is threatening greenhouse horticulture crops worldwide.

RESULTS

In a laboratory trial, gravid females of Amblyseius swirskii, Amblydromalus limonicus, Neoseiulus cucumeris and Transeius montdorensis consumed between 2 and 3.5 first instars of the thrips daily. The predation rates of the phytoseiids tested were lower than those reported when the western flower thrips Frankliniella occidentalis was provided as prey. This predation pattern was confirmed for A. swirskii in a separate trial. In a greenhouse cage trial with sweet pepper plants infested with tobacco thrips, A. swirskii, A. limonicus and N. cucumeris significantly reduced the pest numbers. However, in a commercial Ficus elastica Robusta crop, where A. swirskii and N. cucumeris were introduced weekly, no single predator proved to be sufficiently effective. Larger generalist predators, such as the lacewing Chrysoperla carnea, the predatory thrips Franklinothrips vespiformis, and the predatory bugs Orius laevigatus and Macrolophus pygmaeus were also tested. They reduced populations of tobacco thrips in a cage experiment on sweet pepper. Chrysoperla carnea and F. vespiformis were tested in a commercial Ficus greenhouse and reduced the pest population but were unable to eradicate it.

CONCLUSION

Our results show that the tested mite and insect predators have potential to control tobacco thrips. More research on strategies involving preventative and curative releases of natural enemies, the combination of predatory mites with insect predators or with biopesticides, and the use of supplemental food sources will be needed to curb the spread and damage of T. parvispinus. © 2026 Society of Chemical Industry.

Thrips parvispinus is a thrips species native to the Asian Tropics and has been reported on several crops. We evaluated several predators of T. parvispinus in a range of biosassays. Laboratory and cage trials were conducted on leaves or plants of sweet pepper. The efficacy of selected predatory mite species and insect predators was evaluated in a greenhouse at a Ficus grower.

1. INTRODUCTION

Pest thrips have been a central target of integrated pest management (IPM) in Europe since the first report of the Western flower thrips, Frankliniella occidentalis (Pergande), in 1984. Thrips can cause considerable damage through ovipositing and feeding, even at low population levels. Over the past two to three decades, growers have implemented IPM strategies against thrips, which have resulted in a marked reduction in insecticide applications. Repeated releases of phytoseiid predatory mites and/or anthocorid bugs have proven to be successful against thrips. ¹ Their efficacy has been shown, among others, against onion thrips (Thrips tabaci Lindeman), ² western flower thrips, ³ , ⁴ , ⁵ , ⁶ chilli thrips (Scirtothrips dorsalis Hood) ⁷ and melon thrips (Thrips palmi Karny). ⁸

Over the last decade, biocontrol has been improved with the use of methods that enable growers to pre‐establish and sustain populations of beneficials in the crops through supplemental diets like pollen ⁹ and factitious prey. ¹⁰ , ¹¹ However, with the arrival of new exotic polyphagous thrips species, the established IPM programmes often fail to provide sufficient control, especially in ornamentals. These species include poinsettia thrips (Echinothrips americanus Morgan), Japanese flower thrips (Thrips setosus Moulton), vanda thrips (Dichromothrips corbetti (Priesner)) and tobacco thrips (Thrips parvispinus (Karny)).

Thrips parvispinus is a thrips species native to Southeast Asian countries. It was first described from Thailand (Isoneurothrips parvispinus Karny, 1922), Sumatra, Indonesia (Isoneurothrips jenseni Karny, 1925) and Taiwan (Isoneurothrips pallipes Moulton, 1928; Thrips (Isoneurothrips) taiwanus Takahashi, 1936). The pest has been spreading for the last 20 years and now occurs worldwide. ¹² , ¹³

First reports of T. parvispinus in the Netherlands date back to July 2019. The species was then found on Ficus benjamina L. and Schefflera arboricola (Hayata) Merr. in glasshouse floriculture. ¹⁴ Since then, it has persisted and is becoming an increasing problem in potted plants such as Anthurium, Ficus, Gardenia, Hoya, Mandevilla, Schefflera and Spathiphyllum. Worldwide, the pest has been reported on several other ornamental crops like Citrus, Dahlia, Dipladenia, Gerbera, Ixora, Lobularia, Rosa, Whrightia and orchids. ¹⁴ The pest is also found in fruits and vegetables, such as watermelon, papaya, coffee, strawberry, chili pepper, tobacco, green bean, eggplant, cucurbits and sweet pepper. ¹⁵ , ¹⁶ , ¹⁷ , ¹⁸ , ¹⁹ Currently, T. parvispinus threatens European greenhouse vegetable crops and causes serious injuries in Spanish sweet pepper crops. Nymphs and adults of T. parvispinus mainly inflict direct feeding damage on leaves and growing buds. The pest is also a vector of tobacco streak ilarvirus Ageratum strain (TSV‐Ag) and transmission of the virus from infected tomato pollen to seedlings of Chenopodium amaranticolor Coste & Reynier has been observed. ²⁰ Thrips parvispinus has no quarantine status in Northern Europe. As most growers are not familiar yet with this new thrips species, it is difficult to estimate the extent to which the pest is spreading. This study aimed at determining the potential of existing thrips predators in controlling this increasingly important pest species. We evaluated several predators of T. parvispinus in a range of bioassays. To assess the efficacy of predatory mites, laboratory and cage trials were conducted on leaves and whole plants of sweet pepper (Capsicum annuum L.). Sweet pepper was used as the model host plant for small‐scale experiments because it grows rapidly, is readily available without prior pesticide exposure, and provides a suitable host for both the target thrips pest and its predators. Amblyseius swirskii Athias‐Henriot was selected as the standard predatory mite species. It was mainly chosen for its high temperatures tolerance by Dutch ornamental growers in 2019 when the first pest outbreaks occurred. As predatory mites primarily target thrips eggs and first‐instar larvae (L1), generalist insect predators, capable of feeding on later thrips stages were tested on individual sweet pepper plants in cages. The efficacy of selected predatory mite species and insect predators was further evaluated in a greenhouse at a commercial Ficus elastica L. grower, since T. parvispinus predominantly occurs in ornamental in Northern Europe, and not in sweet pepper.

2. MATERIALS AND METHODS

Young sweet pepper plants cv. Ids (Rijk Zwaan, De Lier, the Netherlands) were used in all laboratory and cage trials. They were sown, transplanted and grown in greenhouses at Biobest N.V. (Westerlo, Belgium) without pesticides.

Two laboratory trials were performed at Biobest Nederland B.V. (De Lier, the Netherlands) in a climate chamber (Sanyo Versatile Environmental Test Chamber, PHC Europe B.V., Etten‐Leur, the Netherlands) under conditions of 25 °C, 70% relative humidity (RH) and a 16 h:8 h (light:dark) photoperiod. Two cage trials took place on growing tables (1.60 × 5.95 m) in a 116 m² greenhouse rented at Vertify (Honselersdijk, the Netherlands). The greenhouse was maintained at 20 ± 3 °C and 70 ± 20% RH. Artificial light was provided 1 h before sunrise and 1.5 h before sunset when light intensity was lower than 250 W, and the daily sum of natural light was lower than 500 J. The plants were provided with a nutrient solution through a drip irrigation system. A grower provided tobacco thrips adults and facilitated two field trials in his commercial greenhouses of F. elastica Robusta in Bergschenhoek (The Netherlands).

The collected tobacco thrips were transported to the laboratory facilities of Biobest Nederland B.V. for identification and rearing. Western flower thrips were provided by Biobest N.V., where they had been reared on bean pods. ²¹ Both thrips species were reared at the laboratory facilities of Biobest Nederland B.V. at a constant room temperature of 21 ± 1 °C. Colonies were maintained on washed pods of green beans (Phaseolus vulgaris L.) in plastic containers (27.5 × 17 × 9 cm) with a lid covered by insect‐proof mesh (10 × 11.5 cm, 25 μm mesh size) to ensure air circulation. Thrips were fed weekly with defrosted pollen of Typha angustifolia L. (Nutrimite™, Biobest N.V.) and fresh bean pods. Pods highly infested with adult thrips, and thus containing eggs, were brushed weekly or daily (depending on the requirements of the trials) and transferred to new rearing containers to create synchronized colonies.

To provide the large number of L1 needed daily for the laboratory predation trial by five predatory mite species, T. parvispinus females were allowed to oviposit for 4 days on sweet pepper leaf discs in the climate chamber. The leaf discs were placed upside down in ventilated plastic cylinders (diameter 4 cm, height 3.2 cm) filled with a layer of moist cotton wool.

All natural enemies used in the trials were commercial products provided by Biobest N.V., except for Franklinothrips vespiformis Crawford, which was supplied by Entocare C.V. The predatory thrips was further reared in the laboratory of Biobest Nederland B.V in ventilated plastic containers (19.5 × 12 × 5 cm), which had an opening (9 × 8.5 cm) in the lid covered with insect‐proof mesh. They were fed with just defrosted eggs of Ephestia kuehniella Zeller and maintained in buckwheat hulls supplemented with plant material for oviposition. The predatory mites tested were either collected from commercial products or reared in the climate chamber on sweet pepper leaf arenas. Synchronized colonies were created following an adapted method of Van Rijn and Tanigoshi. ²² Each sweet pepper leaf was placed upside‐down on a layer of water‐saturated cotton wool in ventilated plastic containers (19.5 × 12 × 5 cm). The leaf was surrounded by strips of wet filter paper, which provided water for the mites and prevented them from escaping the leaf arena. A folded piece of plastic, serving as shelter and oviposition substrate, along with cotton threads as additional oviposition sites, was added to the leaf. Typha angustifolia pollen was supplied as food once a week. Cohorts of predatory mites of the same age were established by transferring the cotton threads.

2.1. Laboratory trials

2.1.1. Predation on T. parvispinus L1 by five predatory mite species on sweet pepper leaf discs

Five phytoseiid species were tested in 20 replicates against T. parvispinus L1: (i) Amblydromalus limonicus Garman and McGregor, (ii) A. swirskii, (iii) Neoseiulus cucumeris (Oudemans), (iv) Transeius montdorensis (Schicha) and (v) Euseius amissibilis Meshkov. A control treatment was included, where no predatory mite was introduced, but only T. parvispinus larvae. The predatory mite species A. limonicus, A. swirskii and T. montdorensis originated from commercial colonies and were reared on astigmatid Carpoglyphus lactis L., whereas N. cucumeris was reared on astigmatid Tyrophagus putrescentiae (Schrank). Euseius amissibilis was obtained from a laboratory rearing on pollen (Nutrimite™). Gravid females (unknown age) were randomly collected with a paint brush and were starved for 16 h at room temperature on sweet pepper leaves placed in ventilated plastic containers (19.5 × 12 × 5 cm). The phytoseiid mites were thereafter transferred individually on a sweet pepper leaf disc that was placed upside‐down on a layer of water saturated cotton wool in a covered plastic tray (9.5 × 6 × 4 cm). The covered tray had an opening of 6.5 × 4 cm in the clear lid that was covered with insect‐proof mesh to allow ventilation. Each leaf disc was covered by a wet filter paper containing a hole of 3.8 cm diameter that provided the mites with water and prevented them from escaping the leaf area. The phytoseiids were provided a folded piece of plastic and bran, which served as both shelters and oviposition substrates. Seven freshly emerged (<6 h) T. parvispinus L1 were collected daily using a fine paintbrush and a dissecting microscope and added to the predatory mites during 3 days. The larvae in the control treatment were refreshed daily as in the other treatments and were provided with the same type of shelters. Living and dead thrips, along with dead phytoseiid females, were eliminated daily. To prevent cannibalism, the eggs of predatory mites were also removed daily. The containers were inspected every 24 h during 3 days to count the number of live and dead thrips and mites. The number of mite eggs was counted before they were removed.

2.1.2. Predation and oviposition on T. parvispinus L1 versus F. occidentalis L1 by A. swirskii on sweet pepper leaf discs in absence and presence of pollen

Because the previous experiment showed that the phytoseiids had lower predation capacity on T. parvispinus L1 than reported for young F. occidentalis larvae, we compared the predation and oviposition rates of A. swirskii when fed on western flower thrips L1 versus tobacco thrips L1 in the presence or absence of pollen. The arena bioassay was conducted in 13 replicates during 4 days, with the same experimental design as the previous experiment. Pollen of T. angustifolia was applied once at the start of the experiment to each sweet pepper leaf disc in the pollen treatments. To simulate the pollen density in commercial crops, the trays containing the leaf discs were placed on the floor and pollen was blown over them using a dusting applicator (Nutrigun, Biobest N.V.), corresponding to the dosage of 0.05 g m² used by commercial growers. One 14‐day‐old adult female of A. swirskii (since egg) was transferred with a brush directly from a synchronized rearing on cattail pollen to the respective experimental units. Each experimental unit received daily, during 3 consecutive days, seven L1 of either T. parvispinus or F. occidentalis. Four additional treatments served as controls for the natural mortality of L1 of both thrips species, either with or without pollen. The predatory mites and thrips larvae were provided with a plastic shelter. The numbers of eggs, living and dead phytoseiid females, and living and dead thrips were counted daily using of a stereomicroscope over a 3‐day period. Living and dead thrips, predatory mite eggs and dead phytoseiid females were removed daily.

2.2. Cage trials

2.2.1. Population dynamics of T. parvispinus on sweet pepper plants in absence and presence of three predatory mite species

Young sweet pepper plants sown on 12 December 2020 at Biobest were transplanted on 3 January 2021 into pots (diameter 18 cm, height 15 cm) filled with growing medium in the greenhouse at Vertify. The plants were placed individually in insect‐proof cages (60 × 60 × 90 cm; Vermandel B.V., Hulst, The Netherlands). The plants did not flower during the experiment. Five adult females of T. parvispinus were released per cage on 26 January. On 2 February, first larval stages of the pest were collected from the rearing using a fine brush and transferred in groups of 13 individuals onto sweet pepper leaf discs. One leaf disc was then deposited on each plant. One week later, 15 additional L1 thrips larvae, 30 pre‐pupae, and a second sweet pepper plant were introduced per cage. Three phytoseiid species (A. limonicus, A. swirskii and N. cucumeris) were tested in six replicates in a complete randomized block design. The predatory mites were released three times, on 12 and 26 February and 5 March, each time with a dosage of 100 predators per cage. Due to the extreme damage caused by T. parvispinus on young sweet pepper plants in the field and the limited efficacy of strategies currently used in Spain (introductions of 10 predatory mites per plant), higher introduction rates were tested here. The approach was based on practices employed by strawberry growers using N. cucumeris for high infestation levels of F. occidentalis. The predatory mites were directly introduced from commercial products supplied by Biobest N.V. along with their carrier material and respective prey mites. The control treatment received no predatory mites. Mite and thrips life stages were counted weekly in situ on all leaves using a magnifier until 12 March.

2.2.2. Population dynamics of T. parvispinus on sweet pepper plants in absence and presence of insect predators

The cage trial was conducted under the same conditions as the previous trial, from 8 November 2022 until 31 January 2023. On 15 November, five 1‐week‐old female T. parvispinus adults were introduced into each cage containing a single 1‐month‐old sweet pepper plant. Four predatory species, the predatory thrips F. vespiformis, the mirid bug Macrolophus pygmaeus Rambur, the green lacewing Chrysoperla carnea (Stephens) and the anthocorid bug Orius laevigatus (Fieber), were tested in three replicates in a complete randomized block design. For each predator species, two introductions of 10 adult individuals were carried out per cage on 13 and 20 December. For the lacewing, first‐instar larvae were introduced. This release rate (100 individuals applied to hot spots of 10 plants, repeated after 1 week) is in line with curative biological control strategies applied in northern European greenhouses, where elevated release rates are used locally to achieve rapid pest control. The rate was chosen to evaluate predator efficacy under high pest pressure and is intended as a targeted local eradication strategy (in hot spots, near greenhouse openings or on infested young plants just arrived from nurseries), rather than a whole‐crop application, which would likely be uneconomical. As the predatory thrips is thelytokous, females were released, while for the predatory bugs, equal numbers of males and females were introduced per cage. The predators and the pest were counted weekly on all leaves with a magnifying glass until 31 January. The plants did not have any flowers during the experiment, as all young buds were removed weekly.

2.3. Field trials

2.3.1. Field trial with A. swirskii, C. carnea and F. vespiformis in a Ficus crop

The first trial took place between 1 October and 17 December 2020 in a 375 m² greenhouse filled with 2‐month‐old Ficus. The diurnal temperature in the greenhouse was maintained at 21 ± 3 °C, while the nocturnal temperature was 18 °C ± 1. The RH was kept at 80% and no artificial lighting was used. Plants were grown in pots (diameter 24 cm, height 24 cm) in a standard peat growing medium. They were irrigated through an ebb‐and‐flow system. At the start of the experiment, plants were approximately 60 cm in height and presented 13 leaves. The plants had been sprayed with insecticides of low persistence (pyridalyl and spinosad) prior to the trial.

The provided greenhouse compartment was divided into five blocks, each comprising five plots of about 55 plants. At the request of the grower, the soil‐dwelling predatory mite Stratiolaelaps scimitus (Womersley) (Acari: Laelapidae) (formerly Hypoaspis miles) was introduced into the growing medium at a rate of 100/m² to target T. parvispinus pupae and sciarids. The predatory mite was evenly distributed so that it would not interfere with the leaf predators' trial. The predatory mite Phytoseiulus persimilis Athias & Henriot was released onto the plants weekly to prevent any spider mite infestation. At the beginning of the experiment, all plants were treated against thrips on 5 and 12 October with a mix of the synthetic insecticides pyridalyl (Nocturn®) and spinosad (Conserve® SC), and a sugar solution to attract thrips. The following treatments were tested in four replicates to assess the effectiveness of the proposed biocontrol strategies: (i) untreated (from week 43, 13 October); (ii) 8 × 50 A. swirskii/plants/week from week 41, 6 October; (iii) 4 × 50 A. swirskii/plants/week (weeks 41, 42, 43, 44) + pollen in weeks 41, 42, 44, 46, 48, 50; (iv) 8 × 2 females of F. vespiformis/plants/week from 6 October; (v) 8 × 20 C. carnea eggs/plants/week from 6 October.

The control treatment did not receive any biocontrol agents against thrips, except for the soil‐dwelling predatory mites. In the pollen plots, pollen of T. angustifolia was blown over the plants weekly at a rate of 500 g/ha on 29 September and 6 October, and later biweekly from 13 October until 15 December using the application device Nutrigun. All commercial biological agents were released with their respective carrier material, which included factitious food. In the A. swirskii + pollen treatment, the predatory mites (mixed stages) were released only four times weekly, from 6 October at a rate of 50 individuals per plant per week. In the other experimental units, 50 A. swirskii, two adult females of F. vespiformis or 20 C. carnea eggs were released per plant every week during 8 weeks from 6 October.

A pre‐count of the number of thrips (adults + larvae) was conducted on five plants per field 1 week before the start of the experiments. The plots were then attributed to treatments in a way evening out the level of infestation among treatment. The efficacy of the tested strategies was assessed biweekly in the greenhouse by counting, using a magnifying lens, the number of living larvae and adults of T. parvispinus, the insect predators observed and the mobile stages of predatory mites on 15 plants per plot. The non‐destructive counts covered five leaves per plant (three in the upper part, one in the middle and one down the plant). No counts were performed on the boarder plants (buffer) of each plot. On 10 December, at the end of the trial, the injury level was assessed on the youngest leaf per plant from 10 plants per plot. A scale from 1 to 8, adapted from the damage evaluation of Van Haperen et al., ²³ was used: 1 indicated a healthy leaf, scores 2 to 7 represented increasing levels of yellow injuries across the leaf surface and 8 corresponded to severe damage characterised by the presence of red scars.

2.3.2. Field trial with A. swirskii and N. cucumeris in a Ficus crop

The experiment was conducted at the same grower in another compartment (208 m²) with 2‐month‐old Ficus between 17 February and 17 March 2021. The greenhouse had a day temperature of 20–32 °C and a night temperature of 18–19 °C. The RH was maintained at 80%. The plants were 60 cm tall (seven leaves) and were grown without artificial light in pots filled with standard potting soil. Before the experiment started, the grower had released A. swirskii weekly until 1 February. The insecticides flonicamid (Teppeki), spinetoram (Exalt) and pyridalyl (Nocturne) were sprayed on 28 December 2020. The allocated crop was divided into four blocks, each divided into five plots of 8.6 m² with 100 F. robusta plants. One hundred S. scimitus/m² were evenly spread over the growing medium in the experimental plots against thrips pupae and fungus gnat larvae (Sciaridae). To prevent spider mites, the predatory mite P. persimilis (10 motiles/m²) was released weekly on the plants. As a preventive measure against aphids, approximately 10 pupae of the gall midge Aphidoletes aphidimyza Rondani/m² were introduced biweekly. To assess the effectiveness of the chosen biocontrol strategies against T. parvispinus, the experiment was set up in four replicates with the five treatments: (i) untreated, (ii) 4 × 20 A. swirskii/plants/week (23/m²), (iii) 4 × 20 N. cucumeris/plants/week. The mixed stages of A. swirskii and N. cucumeris were released in their commercial carrier. The introductions started on 17 February.

The assessments were conducted similarly to those in the first field trial, with a pre‐count and recording of the number of living pest and predators. However, in this trial, the efficacy of the tested strategies was evaluated weekly, but only on the three uppermost leaves of each plant, since T. parvispinus occurs exclusively at the top of Ficus plants. Plant injuries were not scored.

2.4. Statistical analyses

All statistical analyses were performed using RStudio version 2024, 12.0 + 467. ²⁴ A significance level of α = 0.05 was applied to all tests.

Prior to analysis, data were checked for normality using the Shapiro–Wilk test. Homogeneity of variances among treatment groups was assessed using Levene's test (for non‐normally distributed data) or Bartlett's test (for normally distributed data).

Predatory mite predation and oviposition data from the laboratory tests with five phytoseiid species on thrips larvae did not meet the assumptions of normality, nor did the number of eggs laid by A. swirskii on T. parvispinus and F. occidentalis larvae in the second experiment. Therefore, a non‐parametric Kruskal–Wallis test was used to compare mean oviposition and predation rates across treatments. Pairwise Wilcoxon tests with a Bonferroni adjustment were conducted to identify significantly different treatment pairs. In these trials, dead mites or those that escaped from the arena were excluded from the analysis. Additionally, oviposited eggs counted on the first day of the experiment were excluded to remove the effects of previous diet when predatory mites were not starved before the trial. ⁴ We observed no mortality of thrips in the untreated controls. Therefore, no adjustments were needed in the statistical analysis. Data from the predation test of A. swirskii on T. parvispinus and F. occidentalis that met the assumptions of normality and homoscedasticity were analysed using analysis of variance (ANOVA). A non‐parametric Kruskal‐Wallis test was used to analyse the oviposition data.

To assess the effect of predatory mites and insect predators on T. parvispinus in cage trials and field experiments, we applied generalised linear mixed models (GLMMs). A generalised linear model (GLM) was used to analyse plant damage. Thrips and predator densities were analysed among treatments, with treatment and time as fixed factors and replicate as a random factor to account for repeated measures.

Overdispersion was tested by examining the ratio of residual deviance to residual degrees of freedom and using the dispersiontest() function from the AER package. If overdispersion was detected, a negative binomial model was used. Treatment significance was evaluated using a chi‐square test (drop1) and post hoc pairwise comparisons were performed using Tukey's honest significant difference test or the glht() function, implemented with the emmeans package. ²⁵ The compact letter display method was applied for visualisation, where treatments sharing the same letter were not significantly different, while different letters indicated significant differences.

3. RESULTS

3.1. Laboratory trials

3.1.1. Predation on T. parvispinus L1 by five predatory mite species on sweet pepper leaf discs

All tested predatory mite species consumed the first larval stage of T. parvispinus (Fig. 1), although there were differences among the species (Kruskal–Wallis χ ² ₄ = 35.54, P < 0.001). Amblyseius swirskii, N. cucumeris and T. montdorensis killed between 2.2 and 2.6 thrips larvae/day (Fig. 1); Amblydromalus limonicus showed the highest predation rate (3.3 larvae/day). This rate was significantly different only from that of E. amissibilis, which killed 0.5 larvae daily, considerably fewer than all the other phytoseiid species.

Figure 1.

Daily consumption (± standard error) of first‐stage larvae of Thrips parvispinus by five phytoseiid mites in a leaf disc assay. Different letters indicate a significant difference in the number of eaten thrips larvae between the treatments.

The differences in oviposition (Fig. 2) were more pronounced between the species (Kruskal–Wallis χ ² ₄ = 41.58, P < 0.001). Oviposition rates ranged from 0.2 eggs/day (E. amissibilis) to 1.8 eggs/day (A. limonicus) (Fig. 2). Amblydromalus limonicus laid significantly more eggs than the other predatory mite species tested, and the difference in oviposition was also significant between N. cucumeris and E. amissibilis.

Figure 2.

Daily oviposition rate for gravid mites fed first‐stage larvae of Thrips parvispinus in a leaf disc assay. Different letters indicate a significant difference in the number of eggs between the treatments.

3.1.2. Predation and oviposition on T. parvispinus L1 versus F. occidentalis L1 by A. swirskii on sweet pepper leaf discs in absence and presence of pollen

The results of the ANOVA confirmed a highly significant effect of treatment on prey consumption (ANOVA: F _(3,48) = 12.16, P < 0.001). Amblyseius swirskii killed on average 1.7 more first larval stages of F. occidentalis per day (3.7 L1) than larvae of T. parvispinus (2.2 L1) (Fig. 3(a)). Amblyseius swirskii consumed similar numbers of larvae of F. occidentalis or T. parvispinus regardless the supplementation of pollen during the 2‐day observation period (3.5 F. occidentalis L1 without pollen and 3.7 with pollen, 2.2 T. parvispinus L1 without pollen and 2.1 with pollen). Pollen had thus no impact on predation (Fig. 3(a)). However, pollen supply significantly increased mean oviposition by a factor 2 (Fig. 3(b)) compared to a diet on T. parvispinus alone (Kruskal–Wallis χ ² ₃ = 15.19, P = 0.0016). Adding pollen to a diet of F. occidentalis raised also mean oviposition by a factor 1.5 compared to the thrips diet alone, but this difference was not statistically significant (Fig. 3(b)). Oviposition did not differ significantly whenever the predatory mite was fed on either one of the two thrips species alone or in combination with pollen.

Figure 3.

Predation (a) and oviposition (b) of Amblyseius swirskii (A.s.) on first larval stage of Frankliniella occidentalis (F.o.) versus first larval stage of Thrips parvispinus (T.p.) with and without supply of pollen. Different letters indicate a significant difference between the treatments.

3.2. Cage trial

3.2.1. Population dynamics of T. parvispinus on sweet pepper plants in absence and presence of three predatory mite species

All three predatory mite species survived and reproduced when fed with T. parvispinus on the sweet pepper plants, although more A. limonicus and A. swirskii were observed (Fig. 4) (χ ² ₂ = 142, P < 0.001). Neoseiulus cucumeris had a significative lower relative abundance from 4 March compared to the two other species.

Figure 4.

Population dynamics of the average number of predatory mites (± standard error) per cage containing two sweet pepper plants over a period of 4 weeks. Different letters indicate a significant difference in the number of mites between the plants treated with the predators and the control plants (GLMM over all weeks, P < 0.05).

Thrips parvispinus numbers increased rapidly in the cages where no predators were introduced (Fig. 5), reaching more than 500 thrips per cage of two plants 4 weeks after the start of the experiment. The GLMM statistical analysis revealed that all three phytoseiid species significantly reduced thrips numbers compared to the control (χ ² ₃ = 524.83, P < 0.001). Predatory mite densities were inversely related to thrips densities in all cases. Amblydromalus limonicus and Amblyseius swirskii had a significantly greater impact on the pest population dynamics than N. cucumeris. By the end of the trial, there were, respectively, 9.2, 6.7 and 1.6 times fewer thrips in the cages treated with the predators compared to the control.

Figure 5.

Population dynamics of Thrips parvispinus per cage containing two sweet pepper plants for 4 weeks. Different letters indicate a significant difference in the average number of thrips (± standard error) between the plants treated with predatory mites and the control plant (GLMM over all weeks, P < 0.05).

3.2.2. Population dynamics of T. parvispinus on sweet pepper plants in absence and presence of insect predators

Thrips parvispinus reached the highest density (250 per cage) in the control cages without predators (Fig. 6) (χ ² ₄ = 40.87, P < 0.001). All predators significantly affected the development of the pest compared to the control. The green lacewing larvae had the most rapid effect, reducing thrips numbers to below 10 per cage as early as the second week after their release. They maintained the pest at significantly lowest levels throughout the entire experiment; however none of the lacewing larvae reached adulthood. The effect of the predatory thrips and the mirid bug was clearly visible 4 weeks after their introduction, and they also controlled T. parvispinus during the last 2 weeks of the trial. Both predators managed to reproduce on the pest, but their density per plant remained low. At the end of the experiment, 6 weeks after the last predator release, we found a maximum of 10 predators per cage (an average of 6.7 F. vespiformis and 7 M. pygmaeus). The adults of O. laevigatus did not survive beyond the first week and reproduced poorly, as expected in the absence of flowers. Only one to four nymphs per cage were observed 2 weeks after the adults' introduction, and this pattern persisted until the end of the trial. Orius laevigatus did not fully control the pest, but reduced the population by a factor 2.5. Its effect over the weeks was not statistically different from that of the predatory thrips and the mirid bug throughout the entire experiment (Fig. 6).

Figure 6.

Population dynamics of Thrips parvispinus on sweet pepper plants. Different letters indicate a significant difference in the average number of thrips (± standard error) between the plants treated with predatory mites and the control plants (GLMM over all weeks, P < 0.05).

3.3. Field trials

3.3.1. Field trial with A. swirskii, C. carnea and F. vespiformis in a Ficus crop

There was a significant difference in the number of A. swirskii on plants between the treatment with eight introductions of the predator and the treatment with four introductions combined with pollen supplementation (χ ² = 76.88, P < 0.001) (Fig. 7). In the treatment with pollen we recorded 2.6 times more predatory mites.

Figure 7.

Population dynamics of Amblyseius swirskii on Ficus plants for 8 weeks. Different letters indicate a significant difference in the number of predatory mites between the plants treated with predators with and without pollen (GLMM over all weeks, P < 0.05).

The number of T. parvispinus adults on the crop started to increase on 5 November, 24 days after the last application of the synthetic insecticides. Significant differences in thrips numbers were found between the treatments (χ ² ₄ = 388.58, P < 0.001). The number of T. parvispinus was significantly higher in the control (Fig. 8). The number of thrips in the treatments with the predatory thrips and lacewing eggs stayed low until 18 November, but increased over time to reach the unacceptable level of 7.6 and 7.8 thrips per plant respectively. Nonetheless, at the end of the experiment, pest pressure was 31% lower than in the control. No significant differences in the number of T. parvispinus were found between these two predators. Predatory thrips and lacewing larvae were observed sporadically. One and six larvae of C. larvae were counted on 22 October and 5 November, respectively, while one and two larvae of F. vespiformis were found on 18 November and 3 December, respectively. On 17 December, seven larvae and one adult of F. vespiformis were recorded. Both predators performed significantly better than the treatments with A. swirskii. Although the population levels of A. swirskii increased faster in the presence of pollen and reached ca. 1.7 mites per leaf (Fig. 7), more thrips and damage were recorded (about twice more on 17 December) when pollen was applied compared to plots were the predatory mite was repeatedly released. However, plant damage was not statistically significantly higher in the presence of pollen.

Figure 8.

Population dynamics of Thrips parvispinus on Ficus plants for 8 weeks. Different letters indicate a significant difference in the average number of thrips (± standard error) between the plants treated with predatory mites and the control plants (GLMM over all weeks, P < 0.05).

Analysis of plant damage ratings on 10 December showed a significant effect of the predators treatments (GLM, χ ²4 = 199.53, P < 0.001) with mean thrips damage scores between 2.5 (C. carnea) and 4.55 (A. swirskii + pollen) for the predators and 6.6 for no predators controls (Fig. 9).

Figure 9.

Average damage scores (± standard error) caused by Thrips parvispinus on Ficus leaves. Different letters indicate a significant difference in the injury level caused by thrips among treatments.

3.3.2. Field trial with A. swirskii and N. cucumeris in a Ficus crop

Population densities of the predatory mites and T. parvispinus are shown in Figs 10 and 11. Amblyseius swirskii was recorded more frequently compared with N. cucumeris from 2 March (χ ² = 30.6, P < 0.001), but numbers remained low (Fig. 10). No predators were observed in control plants. As the predators were released weekly, it is not possible to tell if they reproduced on the plants. No eggs were found on the assessed leaves. Total numbers of thrips never exceeded nine per plant when leaf predatory mites were introduced whereas we found up to 16 in the control (Fig. 11). However, sufficient thrips control was not provided. The number of thrips was only halved by both mite species (i.e., 0.5 ± 0.25 thrips/plant) at the end of the experiment (χ ² ₂ = 49.96, P < 0.001). The damage represented no problem, as new growth quickly replaced the light‐damaged top leaf. However, as the pest populations were increasing throughout the greenhouse, the use of synthetic insecticides became necessary.

Figure 10.

Population dynamics of predatory mites on Ficus plants for 5 weeks. Different letters indicate a significant difference in the number of predatory mites between the plants treated with predators and the control plants (GLMM over all weeks, P < 0.05).

Figure 11.

Population dynamics of Thrips parvispinus on Ficus plants for 5 weeks. Different letters indicate a significant difference in the number of thrips among treatments (GLMM over all weeks, P < 0.05).

4. DISCUSSION

In our laboratory and cage trials, the predatory mites species A. limonicus, A. swirskii, E. amissibilis, N. cucumeris and T. montdorensis, as well as the lacewing C. carnea, the predatory thrips F. vespiformis, and the predatory bugs Orius laevigatus and M. pygmaeus were able to feed on T. parvispinus.

The results presented in this study showed that the five predatory mite species tested can feed and lay eggs on the first larval stage of the pest. Our data regarding predation on first larval stages of T. parvispinus show that A. limonicus, A. swirskii, N. cucumeris and T. montdorensis feed on two to three larvae per day. Out of the species tested, A. limonicus showed the highest predation and oviposition rates, although the differences in predation were not statistically significant between A. swirskii, N. cucumeris and T. montdorensis. A recent laboratory study showed also a low predation level of L1 T. parvispinus by the species Euseius degenerans (Berlese), with an average of 1.4 killed out of 15 offered during four days of exposure, whereas predation by A. swirskii exceeded 7. ²⁶ Amblydromalus limonicus has previously shown to be more effective than A. swirskii, Euseius ovalis (Evans) and N. cucumeris for F. occidentalis control in cucumber. ²⁷ However, it has not yet been widely used due to its relatively high cost. The results of our experiment differ from reported predation rates on young F. occidentalis larvae. The predation capacity of the phytoseiids on L1 T. parvispinus was merely half of what has been reported in publications on L1 F. occidentalis. At 25 °C, A. limonicus fed on 6.9 F. occidentalis L1/day, ⁴ N. cucumeris 5.8 to 6/day, ²⁸ , ²⁹ A. swirskii 4 to 4.9/day, ²⁹ , ³⁰ T. montdorensis 4.4/day ³¹ and E. assimibilis 2.6/day. ³²

Dutch potted‐plant growers and their crop protection advisers had already suspected that T. parvispinus is more difficult to control than F. occidentalis with predatory mites, as most of their IPM programmes in different crops have failed. We confirmed this difference in predation rates in the trial with A. swirskii, when offered either young T. parvispinus larvae or F. occidentalis. In this study, more F. occidentalis larvae were consumed per day, regardless of whether pollen was applied. Thrips parvispinus thus appears to be more difficult for phytoseiids to detect, capture or feed on, which is consistent with the findings of Beretta et al. ³³ Certain thrips, like E. americanus, species possess some physical traits that deter predators or they exhibit more pronounced defensive behaviour. ³⁴ , ³⁵ Thrips often use different mechanisms to defend themselves, such as ‘wagging’ ³⁶ or jerking their abdomen. ³⁷ , ³⁸ Large thrips often perform this physical counter‐attack more effectively than smaller species. ³⁹ Sometimes thrips also release a droplet of rectal fluid which deters predatory mites ⁴⁰ , ⁴¹ and acts as an alarm pheromone towards conspecifics. ⁴⁰ , ⁴¹ , ⁴² Eggs, second‐instar larvae and thrips pupae were not tested in this study. In general, second‐instar larvae and pupae can also be consumed, even though to a lesser extent. ³⁸ , ⁴³ , ⁴⁴ The predation of thrips eggs by phytoseiids has long been overlooked in biocontrol strategies, as the capacity to feed on first‐instar thrips has traditionally been the primary parameter used to evaluate the performance of these predators. ³⁹ However, Vangansbeke et al. ⁴⁵ , ⁴⁶ found mortality rates of six F. occidentalis eggs embedded in leaf tissue/24 h for A. limonicus, five for E. amissibilis, four for A. swirskii, three for N. cucumeris and two for T. montdorensis. Nguyen et al. ⁴⁷ reported predation by A. swirskii of five to six F. occidentalis eggs per day. Consumption of thrips eggs can be important in thrips management as it controls the pest before larvae cause feeding damage, and it can be even more valuable for biocontrol of thrips species with pronounced defensive larval behaviour.

Our trial results at plant level highlight the importance of predators' establishment on plants. On individual sweet pepper plants in cages, the best results against T. parvispinus were obtained on plants where the predatory mites established best. The results clearly show that the predators were effective in suppressing T. parvispinus. However, comparison between the predator species should be interpreted with caution due to our small sample size.

Predators tend to establish better in sweet pepper crops compared to potted ornamental plants. Indeed, the persistence of the predatory mites A. swirskii and N. cucumeris on Ficus was poor, requiring repeated releases. Only a few predatory mites were found on Ficus, where T. parvispinus is particularly problematic (<0.3 A. swirskii per leaf and <0.03 N. cucumeris per leaf after a low dose rate of four introductions of 20 individuals per plant, one A. swirskii per leaf after the high dose rate of eight introductions of 50 individuals per plant). It is not surprising that T. parvispinus develops better in certain potted ornamentals, where biological control agents fail to establish, than in greenhouse vegetable crops where beneficials are more readily present. This disparity can be attributed to the absence of suitable oviposition sites, such as acarodomatia, which leaves phytoseiids struggling to persist on smooth stems and leaves. This may be aggravated by the shorter stature of the plants, the often harder epidermis and the often extreme temperature ranges and low humidity.

To support the establishment of predatory mites in crops before the development of thrips, T. angustifolia pollen is sometimes used in IPM programmes. ¹¹ Our laboratory test has once again demonstrated that this pollen is a suitable food source for A. swirskii. Supplying pollen enhanced the oviposition of the predator in the laboratory without reducing its predation on either T. parvispinus or F. occidentalis. In the experiment at the Ficus grower, the application of cattail pollen as an additional food source improved the maintenance of A. swirskii populations and resulted in better biological control of T. parvispinus compared to control treatments, but not compared to weekly introductions of the predator without pollen. Based on our results, we suggest that high inoculative releases of predatory mites early in the crop cycle can contribute to a preventative control of T. parvispinus. In Ficus, thrips numbers were reduced by a factor of five at the high release rate of A. swirskii and by a factor of two at the low release rate. The tested insect predators achieved a greater reduction in thrips number, but resulted in levels of plant damage that were not statistically different. However, although all tested predators were able to reduce thrips populations and damage in Ficus, they did not control the pest sufficiently to keep damage below economically acceptable levels, and the application of pesticides remained necessary. Further studies are now required to test combinations of both predatory mites and insect predators, as well as the integration of biopesticides, to determine whether such a strategy could provide adequate control of T. parvispinus.

In our search for ‘more effective’ thrips predators, the predatory bugs O. laevigatus and M. pygmaeus, the lacewing C. carnea and the predatory thrips F. vespiformis have proven to be promising candidates in a cage trial on sweet pepper. To our knowledge, no data have been published on the predation rates of O. laevigatus, M. pygmaeus and C. carnea on T. parvispinus. In previous laboratory studies, ⁴⁸ we found that first instar, second instar and adults of F. vespiformis consume 4.6, 7.5 and 11.6 first instars of T. parvispinus per day, respectively, and 2, 6.6 and 8.7 eggs embedded in sweet pepper leaflets. Franklinothrips vespiformis adults exhibited a daily predation rate of 6.75 T. parvispinus adults, which was similar to the 6.5 F. occidentalis consumed per day by this predator. Similar predation rates have been reported for another predatory thrips species, F. megalops (Trybom), which has been found to occur spontaneously in thrips‐infested crops (M. Porcel et al., unpublished). In comparison to predatory thrips, the first larval stage of the lacewing killed an average of 30.6 first instars of T. parvispinus daily (Pijnakker et al., unpublished). Orius laevigatus has not yet been tested against T. parvispinus in our laboratory, but Mouratidis et al. ⁴⁹ demonstrated that females of O. laevigatus and O. majusculus (Reuter) killed 18 and 20 F. occidentalis adults, respectively, within 24 h, which is in line with earlier findings in laboratory studies ⁵⁰ , ⁵¹ and that this rate doubled when the thrips species E. americanus or T. setosus were offered as prey. Saito & Buitenhuis ⁵² reported that a single adult female of another Orius species, O. insidiosus (Lay), can kill about 21 adult female T. parvispinus out of 40 within 24 h. Comparable rates were observed in India for another anthocorid bug, Blaptostethus pallescens Poppius, where adult females consumed an average of 25.5 thrips when 50 were offered. ⁵³ The efficacy of Macrolophus pygmaeus in reducing thrips (F. occidentalis) populations in sweet pepper crops has already been demonstrated. ⁵⁴ , ⁵⁵ Leman et al. ⁵⁶ reported that, on average, 21.6 out of 50 adult E. americanus were consumed daily in a setting where whiteflies were also present. The predatory bug is commonly released alongside O. laevigatus in sweet pepper greenhouses in northern Europe due to its generalist predatory behaviour. However, it is not used in ornamental crops because it can sometimes damage flowers (e.g., gerbera), and its establishment is not always successful because some cut flowers or potted plants are unsuitable for reproduction. Adding mirids to biocontrol strategies could contribute to the management of T. parvispinus, possibly in combination with the use of banker plant systems like Verbascum thapsus ¹¹ or Verbena spp. ⁵⁷ when the crop is not suitable for their reproduction. Other mirid species may be considered, such as Nesidiocoris tenuis (Reuter), depending on their geographic distribution, or species that pose less risk of plant damage, such as Dicyphus spp.

Overall, the efficacy of the tested insect natural enemies in vegetable crops will depend on their abundance, established or released, at the time the pest appears. While predator numbers declined over the time of our cage experiment, this is not unusual for studies of limited duration. This decline may be attributable to the common phenomenon in which some predators fail to establish likely due to food limitation, combined with a delay in their reproduction. These factors may be further compounded when the prey is suboptimal for both feeding and reproduction. Several valid methods have been proposed to boost and maintain predator's populations. ¹¹ , ⁵⁸ , ⁵⁹

For ornamental growers, we expect that pest will be effectively managed by incorporating biopesticides into their strategy alongside natural enemies, whether used in combination or separately. Future studies should therefore focus on the combination of natural enemies and biopesticides, evaluating their efficacity, persistence and compatibility with natural enemies. The optimal time for spraying should be determined to allow growers to keep the pest below the crop‐specific economic damage threshold. The choice of predators will depend on their affinity for the crop, their compatibility with other biological control agents, their efficacy and the costs of the overall release strategy. Neoseiulus cucumeris and Transeius montdorensis are currently the least expensive options. Among commercially available soil‐dwelling predatory mite species, Stratiolaelaps scimitus is the most commonly used. The lacewing C. carnea, compared to F. vespiformis and Orius laevigatus, has the added benefit of feeding on spider mites, mealybugs and aphids, which are also common pests in Ficus. However, establishment of lacewings in ornamentals is negligible, and biocontrol strategies would require repeated releases. In the experiment at the Ficus grower, neither lacewings nor predatory thrips established, although our results indicated limited reproduction of F. vespiformis when pest levels increased. It may be valuable to further evaluate the predatory thrips using supplementary food source.

In conclusion, our study suggests that the tested mite and insect predators have potential for controlling T. parvispinus. Integrating them into IPM strategies, supported by alternative food sources, could improve their establishment and efficacy in crops. However, it remains important to evaluate whether the selected natural enemies may interfere with the biological control of other pests at the crop level.

ACKNOWLEGMENTS

The authors are grateful to the following colleagues for providing technical assistance: Diana Overgaag, Peggy Bogaerts, Ilse Jacobs, Koen Merkus and Marvin Koot. We would to thank Martijn Roos for allowing us to conduct our trials in his production greenhouses. His invaluable assistance and access to his facilities greatly contributed to the success of this research. We truly appreciate his willingness to collaborate and his commitment to advancing knowledge in the field.

CONFLICT OF INTEREST

All authors are employed by Biobest and declare no conflict of interest.

DATA AVAILABILITY STATEMENT

Research data are not shared.