Thrips (Thysanoptera) are small, slender “fringe-winged” insects, of which many species are plant feeders, and some are significant pests of crops and commodities worldwide (Childers 1997). Thrips in the genus Frankliniella (Thysanoptera: Thripidae) (flower thrips) feed on swollen buds, open flowers, and developing fruits of many vegetables, fruits, and ornamentals, therein causing necrosis, cellular collapse, distortion, discoloration, silvering, or fruit abortion (Childers & Achor 1991; Childers 1997; Shipp et al. 2000). In strawberry, Frankliniella spp. and other genera have been linked to flower damage and fruit bronzing and scarring in many production regions, including the United States, Europe, Australia and Japan (Steiner & Goodwin 2005). The cosmopolitan Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) may have the greatest economic impact on strawberry, but relationships between F. occidentalis density and crop damage are variable (Steiner & Goodwin 2005; Coll et al. 2006; Atakan 2011). Frankliniella occidentalis has been established in Florida, USA, since 1982 and has affected strawberry production in the state since 2004 (Kirk & Terry 2003; Whidden 2004). In addition, the native Frankliniella bispinosa Morgan (Thysanoptera: Thripidae) occurs in strawberry in the southern half of Florida and likely causes flower and fruit damage, as it does in blueberry and bell pepper (Reitz et al. 2003; Rhodes and Liburd 2011). Frankliniella spp. can be difficult to manage because of their cryptic behavior, rapid reproduction, and the ability of F. occidentalis to develop resistance to insecticides (Immaraju et al. 1992; Broadbent & Pree 1997). Therefore, new approaches and tools for thrips management are needed for Florida strawberries.

Entomopathogenic nematodes have been widely assessed for suppression of life stages of agricultural pests that are spent primarily in the soil, where free-living infective juvenile nematodes occur (Gothro 2000). When the host insect's habitat is suitably humid and cryptic, entomopathogenic nematodes have shown some efficacy for suppression of above-ground pests (Olthof & Broadbent 1992; Williams & Walters 2000; Shapiro-Ilan et al. 2006). Several entomopathogenic nematode species attack soil-dwelling pupae of F. occidentalis (Ebssa et al. 2001), and Steinernema feltiae (Filipjev) (Rhabditida: Steinernematidae) is capable in the laboratory of causing mortality to the larval and pre-pupal stages (Buitenhuis & Shipp 2005). Wardlow et al. (2001) reported effective control of F. occidentalis with weekly applications, but Buitenhuis & Shipp (2005) reported no reduction of F. occidentalis after a foliar application in chrysanthemum, Dendranthema grandiflora Tzvelev (Compositae), flowers. Factors that affect entomopathogenic nematode efficacy include the innate infectivity of nematode species, differences in susceptibility of thrips developmental stages, differences among thrips species, the complexity of flowers and degree of concealment for entomopathogenic nematodes afforded by flowers, and addition of adjuvants that may facilitate entomopathogenic nematode movement and host finding by reducing rates of drying and desiccation (Kaya & Gaugler 1993; Broadbent & Olthof 1995; Baur et al. 1997; Buitenhuis & Shipp 2005; Cuthbertson et al. 2005).

Fig. 1.

Least square means (± 95% confidence intervals) for (A) adult and (B) larval thrips (Frankliniella bispinosa) per 10 strawberry flowers from research plots near Balm, Florida, sprayed 26 Feb, and 1, 5, and 9 Mar 2016 with Steinernema feltiae or insecticides. Means in each panel with the same letter are not significantly different (Tukey's HSD test, α = 0.05) (Experiment 1).

In addition to non-chemical controls, new insecticides with novel modes of action will be useful for developing an effective management program for thrips in strawberries. The sulfoximines, in particular sulfoxaflor, act on insect nicotinic receptors, similar to other insecticide classes (spinosysns, neonicotinoids), but have a number of different structure-activity relationships that confer a unique mode of action (Watson et al. 2011; Sparks et al. 2013). Sulfoxaflor has potent insecticidal activity on many sap-feeding insects, and has not exhibited crossresistance when tested on imidacloprid-resistant strains of sweetpotato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) and brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) (Babcock et al. 2011). For thrips control, 4-insecticide rotations including an application of sulfoxaflor were as effective as rotations without sulfoxaflor for suppression of flower thrips species in Florida strawberries; however, sulfoxaflor-specific data was not presented (Cleuver et al. 2016). Sulfoxaflor reduced melon thrips, Thrips palmi Karny (Thysanoptera: Thripidae), in eggplant (Seal 2012); citrus thrips, Scirtothrips citri (Moulton) (Thysanoptera: Thripidae), in navel oranges and southern highbush blueberries (Haviland & Rill 2015; Van Steenwyk et al. 2016); and F. occidentalis in iceberg head lettuce (Natwick & Lopez 2014). Sulfoxaflor may be an effective alternative to commonly used insecticides for thrips in Florida strawberries, such as spinetoram and acetamiprid, but further testing is needed.

Thrips have become a major challenge for Florida producers of winter (Nov–Mar) strawberries (Cluever et al. 2016). As seasonal temperatures have been above historical average and freezing events rare in recent years in strawberry producing areas (FAWN 2017), flower thrips populations do not decline but remain high throughout the season. Wild hosts are common around fields; wild radish, Raphanus raphanistrum L. (Brassicaceae), seems to be increasing in abundance and produces flowers almost continuously throughout the strawberry season, acting as a reservoir for F. bispinosa (Cleuver et al. 2016). Chilli thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae), is a recent Florida invader of subtropical/tropical origin (Dickey et al. 2015) that damages new foliage of young strawberry plants and is having an increased impact with fall and winter temperatures, generally above-normal in recent years. Furthermore, the same insecticides are typically effective on flower and chilli thrips, so growers must carefully manage the timing of a limited number of applications. The objective of this study was to evaluate foliar applications of S. feltiae and the insecticide sulfoxaflor in Florida strawberries for suppression of flower-inhabiting thrips, and on strawberry yield. This research was conducted in an effort to provide Florida strawberry growers with additional tools to rotate with existing products and practices for thrips control.

Table 1.

Analysis of variance results and means (95% confidence limits) for thrips (Frankliniella bispinosa) and insidious flower bugs (Orius spp.) per 10 flowers, and thrips-damaged strawberries from plots sprayed with Steinernema feltiae, spinetoram, or both treatments 26 Feb to 9 Mar 2016 near Balm, Florida (Experiment 1). Means within columns followed by the same letter are not significantly different (Tukey's HSD, α = 0.05).

Materials and Methods

Two experiments to test efficacy of insecticides and an entomopathogenic nematode on flower thrips were conducted in plots of winter strawberries at the Gulf Coast Research and Education Center, Balm, Florida, USA (27.7621°N, 82.2258°W). Bare-root strawberry transplants (cv. ‘Radiance’) were set 14 Oct 2015 at 38 cm spacing in raised, black plastic-mulched beds at 1.2 m spacing. Fumigation with Telone® C-35 (1,3-dichloropropene + chloropicrin) occurred at bed formation on 20 Aug 2015. Plants were overhead irrigated for 10 d following transplanting and drip-irrigated and fertigated with 0.27 and 0.34 kg N per d from Nov to Jan and Feb to Apr, respectively. Round-up® (glyphosate) and Chateau® (flumioxazin) were applied to row aisles before transplanting to control weeds. Plants received weekly applications of fungicides and occasional applications of DiPel® DF (Bacillus thuringiensis, subsp. kurstaki) Berliner (Bacillales) to control lepidopteran larvae.

Each strawberry plot was a 10 m double-row, single bed (50–54 plants). Plots were laid out in 5 adjacent beds in a randomized complete block design, with a 1 m and 2 m unplanted buffer on the ends of plots within blocks and between blocks, respectively. Experiment 1 was conducted on the first, third, and fifth row, and Experiment 2 on the second and fourth row, so that there were unsprayed strawberry rows between plots for both experiments.

Treatments were applied at 940 L per ha with a CO2-powered backpack sprayer (R & D Sprayers, Opelousas, Louisiana, USA) at 60 PSI using a hand-held wand sprayer with 2 nozzles without filters. Insecticides, entomopathogenic nematodes, and controls (water) were mixed with the non-ionic surfactant, Induce® (0.25% v/v) (Helena Chemical Co., Collierville, Tennessee, USA). Applications were made 1 h prior to sunset to facilitate entomopathogenic nematode survival in flowers. Treatment efficacy was evaluated by randomly selecting 10 open flowers per plot and quickly placing them in plastic centrifuge tubes (50 mL) half-filled with 70% ethanol. In the laboratory, flowers were poured from tubes into Petri dishes and each flower was held with forceps and washed with additional ethanol before discarding it. Adult and larval thrips and predatory insidious flower bugs (Orius spp.) (Hemiptera: Anthocoridae) in the ethanol were identified and counted under a stereomicroscope. Yield was evaluated by harvesting all ripe strawberries in each plot and evaluating for thrips-related damage, such as bronzing, scarring, or cracking.

Table 2.

Analysis of variance results and means (95% confidence limits) for thrips (Frankliniella bispinosa) and insidious flower bugs (Orius spp.) per 10 flowers, and thrips-damaged strawberries from plots sprayed with Steinernema feltiae, spinetoram, or sulfoxaflor 2 to 24 Mar 2016 near Balm, Florida (Experiment 2). Means within columns followed by the same letter are not significantly different (Tukey's HSD, α = 0.05).

Results

EXPERIMENT 2

Numbers of total and larval thrips were affected by treatments, but adults were not affected (Table 2). There were about twice as many larval thrips with applications of S. feltiae compared to sulfoxaflor, and about half as many larvae when comparing spinetoram to sulfoxaflor (Table 2). Even though there was not a significant treatment by date interaction, adult thrips numbers appeared to be reduced to a greater extent in plots treated with spinetoram and sulfoxaflor compared to S. feltiae-treated and control plots. However, after 7 Mar 2016 adult thrips numbers were similar among treatments (Fig. 2A). Larval thrips numbers were reduced by spinetoram and sulfoxaflor as compared to S. feltiae treatments, and control was achieved for almost 2 wk following first application on 3 Mar 2016 (Fig. 2B). The number of insidious flower bugs was affected by treatment, with more than twice as many in control than spinetoram and sulfoxaflor plots (Table 2). Yield was not affected by the treatments (F3,9 = 1.4; P = 0.303). Thrips-damaged fruit was affected by treatment, with almost zero damage when spinetoram was applied, compared to about 1% when sulfoxaflor was applied and 3 to 4.5% in S. feltiae and control plots (Table 2).

Fig. 2.

Least square means (± 95% confidence intervals) for (A) adult and (B) larval thrips (Frankliniella bispinosa) per 10 strawberry flowers from research plots near Balm, Florida, sprayed 3, 7, and 16 Mar 2016 with Steinernema feltiae and 3 and 16 Mar 2016 with insecticides. Treatments were applied and reapplied when total thrips counts exceeded 5 per flower. Means in lower panel with the same letter are not significantly different (Tukey's HSD test, α = 0.05) (Experiment 2).

Fig. 3.

Hourly temperature (left y-axis), rainfall, and relative humidity (right y-axis) 26 Feb to 25 Mar 2016 at Balm, Florida.

Discussion

Our results showed that sulfoxaflor controlled Florida flower thrips and reduced thrips-related fruit damage in Florida strawberry. However, S. feltiae was not effective at reducing or suppressing flower thrips or reducing strawberry damage. As research on management strategies for multiple species of thrips in Florida strawberry progresses, it will be important to rate the relative strengths of insecticides in order to develop optimal season-long rotations. Furthermore, factors affecting or limiting the efficacy and use of biological control organisms need to be explored to enable future research.

Spinetoram is an effective insecticide for control of multiple thrips species in a wide variety of crops, providing rapid-knockdown and sustained suppression of populations (Khaliq et al. 2014; Srivastava et al. 2014; Marasigan et al. 2016). Spinetoram is widely used in Florida strawberry and other horticultural crops, with the result that some F. occidentalis, but not F. bispinosa, populations have recently developed resistance (D. Sprague personal communication). Even though F. occidentalis was not widely reported by growers as a problem in the previous strawberry season, spinetoram is now also routinely used to control S. dorsalis early in the season, when strawberry plants first begin to flower. This study has shown that sulfoxaflor reduces flower thrips, reduces damage to strawberry, and does not adversely affect predatory insidious flower bugs, suggesting that it may be a suitable replacement for spinetoram. However, because the level of flower thrips reduction was not as great for sulfoxaflor as for spinetoram, sulfoxaflor may be better suited as a second application following spinetoram, in lieu of 2 successive spinetoram applications. The composition and order of insecticides is currently being evaluated in a season-long program for control of flower and chilli thrips in Florida strawberry crops.

Treatments of S. feltiae in strawberry plots resulted in no reduction of any thrips life stage or feeding damage. The most common factors limiting efficacy of foliar entomopathogenic nematode applications are susceptibility of the nematodes to ultraviolet light and desiccation (Gaugler & Boush 1978; Arthurs et al. 2004; Shapiro-Ilan et al. 2006). During these experiments, high temperatures and absence of rainfall likely caused significant desiccation and nematode mortality. An additional potential success-limiting factor is that the foliar environment may not provide sufficient support and leverage for S. feltiae to physically penetrate the host's spiracles (Eidt & Thurston 1995; Evans et al. 2015). Control of F. occidentalis with foliar applications of S. feltiae has been discussed (Shapiro-Ilan et al. 2006), although results have been variable (Arthurs & Heinz 2005; Beck et al. 2015). Only F. bispinosa was found in these experiments, and as these congenerics have similar life histories, we expected similar effects of S. feltiae. However, to our knowledge, S. feltiae has not been tested on F. bispinosa in a controlled environment, and subtle behavioral differences between these species may potentially alter their susceptibility to entomopathogenic nematodes. Entomopathogenic nematodes are virulent to soil-dwelling pupae of F. occidentalis (Chyzik et al. 1996; Ebssa et al. 2001; Premachandra et al. 2003), and some entomopathogenic nematodes in foliar applications likely land on the soil. However, in a raised-bed, plastic-mulched strawberry system, Frankliniella spp. are less likely to pupate in soil than on the plastic, under senescing leaves, or on living plant parts where entomopathogenic nematode survival, and thus infectivity rates, are likely to be low. Nematode species and strain may play a role in thrips suppression as well, as 2 strains of H. bacteriophora, for example, conferred very different levels of F. occidentalis control (Chyzik et al. 1996). The entomopathogenic nematode's foraging strategy and the location of the pupae in the soil likely play an important role in host infectivity dynamics (Kaya & Gaugler 1993; Chyzik et al. 1996).

Currently, sulfoxaflor (Closer®) is not registered for use in strawberry in the USA. Registration was cancelled late in 2015, but growers with product may still legally apply Closer®. Pending re-registration of Closer® in strawberry, as has occurred in other crops, growers will regain a valuable, additional tool for thrips insecticide rotation programs. Before entomopathogenic nematodes can be used for thrips management in Florida strawberry production, advancements in commercial delivery methods and application technologies will be necessary. For example, the thrips parasitic nematode, Thripinema nicklewoodi Siddiqui (Tylenchida: Allantonematidae), applied via infected thrips hosts rather than an aqueous suspension, has been shown to infect high numbers of F. occidentalis on foliage and persist for up to 9 generations (Arthurs & Heinz 2006). Overall, an improved integrated approach to thrips management in Florida strawberry is needed, with research focused on developing biological, chemical, and other methods that can be used to provide effective and economical control options.