Thrips (Thysanoptera) cause economic damage to strawberry (Fragaria ananassa Duchesne; Rosales: Rosaceae) crops in many production regions, including the United States, Latin America, Europe, the Mediterranean, Australia, and Japan (Buxton & Easterbrook 1988; González-Zamora & Garcia-Marí 2003; Katayama 2005; Steiner & Goodwin 2005; Coll et al. 2007; Koike et al. 2009; Nondillo et al. 2010). Feeding by Frankliniella (Thripidae) thrips causes abortion of flower and fruitlets as well as bronzing and malformation of fruit (Koike et al. 2009). Globally, the western flower thrips, Frankliniella occidentalis (Pergande), causes the greatest damage to strawberry. Frankliniella occidentalis is a cosmopolitan pest of many horticultural crops (Lewis 1997). It is difficult to manage with insecticides because of its cryptic behavior, its ability to reproduce rapidly, and its tendency to develop tolerance to a broad range of insecticide modes of action (Funderburk 2009; Gao et al. 2012). The spinosyns have been among the most effective insecticides for managing western flower thrips (Funderburk 2009). However, resistance to spinosyns among western flower thrips has been documented (Loughner et al. 2005; Bielza et al. 2007; Zhang et al. 2008). Predatory anthocorids in the genus Orius Wolff (Hemiptera: Anthocoridae) have demonstrated efficacy in suppressing thrips in fruiting vegetables and strawberries if compatible insecticide regimes are employed (Funderburk et al. 2000; Bennison et al. 2011).

Frankliniella occidentalis became established in Florida in 1982 (Kirk & Terry 2003) and was first reported affecting Florida strawberry production in 2004 (Whidden 2004, 2008). However, the predominant thrips species in cultivated and wild plants in the southern portion of Florida, including strawberry-producing areas, is Frankliniella bispinosa Morgan, locally known as the Florida flower thrips (Frantz & Mellinger 1990; Childers & Nakahara 2006). Frankliniella bispinosa, which is native to Florida, is a primary pest of blueberries (Vaccinium corymbosum L., Vaccinium darrowii Camp; Ericales: Ericaceae) (Rhodes et al. 2012) and has been known as an occasional pest of strawberries, tomatoes (Solanales: Solanaceae), citrus (Sapindales: Rutaceae), and other crops in Florida for over a century (Quaintance 1898; Watson 1922; Childers & Achor 1991). Sampling methods and action thresholds for F. occidentalis in strawberry have been developed in various regions (González-Zamora & Garcia-Marí 2003; Katayama 2005; Coll et al. 2007; Nondillo et al. 2009, 2010); however, the comparative economic importance of F. occidentalis, F. bispinosa, and other thrips in Florida strawberry remains relatively unstudied. Thrips species may vary according to the damage they cause and their susceptibility to insecticides and predation (Reitz et al. 2003, 2006; Steiner & Goodwin 2005). Steiner & Goodwin (2005) developed distinct action thresholds for F. occidentalis and Thrips imaginis Bagnall (Thripidae) for hydroponically grown strawberry in Australia.

Frantz & Mellinger (1990) first observed the tendency of F. occidentalis to displace F. bispinosa in intensively sprayed pepper (Capsicum annuum L.; Solanales: Solanaceae) fields in southeast Florida. They attributed this displacement to the use of pyrethroid insecticides (Frantz & Mellinger 2009). Dow AgroSciences voluntarily withdrew spinosyn insecticides from 2 Florida counties from 2008 to 2011 because of evidence that F. occidentalis affecting pepper had become resistant to the material (Hou et al. 2014). Increases in populations of F. occidentalis after the application of pyrethroid insecticides in fruiting vegetables also are associated with the suppression of Orius populations (Funderburk et al. 2000; Ramachandran et al. 2001; Reitz et al. 2003) and the elimination of congeneric competitor species including F. bispinosa (Funderburk et al. 2015).

Strawberries in Florida are grown primarily in Hillsborough County. They are planted in Oct, and overhead irrigation is applied for approximately 10 d to aid in transplant establishment, after which fields are irrigated with drip irrigation. Florida strawberry growers typically apply a “clean-up” spray of a pyrethroid insecticide after the initial period of overhead irrigation. Depending on the severity of the winter weather, thrips establish in strawberry as early as Dec or as late as Mar. Strawberries are typically harvested in Florida from Nov through Apr. Intensive surveys of thrips species associated with strawberry in Hillsborough County have not been carried out before the present study. Frankliniella adults and larvae feed preferentially on pollen and floral parts but will also feed on foliage (Reitz 2009). Damage to flowers and developing fruit directly impacts fruit quality and quantity.

In the spring of 2013, Frankliniella populations reached high densities in strawberry in Hillsborough and adjacent counties, causing significant bronzing to the crop (Smith & Whidden 2014). Growers observed that applications of insecticides, including the spinosyn spinetoram (Radiant SC; Dow Agrosciences, Indianapolis, Indiana), did not consistently reduce the numbers of thrips in the field. In response to concerns that spinetoram was losing efficacy, experiments were carried out at the University of Florida's Gulf Coast Research and Education Center in 2014 and 2015 to evaluate insecticide rotations that emphasized alternative modes of action to spinetoram. The goal was to determine if insecticide programs consisting of only 1 or 2 applications of spinetoram out of 4 weekly sprays (1 spray per week over 4 wk) would be as effective in suppressing thrips as a program with 3 applications of spinetoram and 1 alternative mode of action over a 4 wk period. Active ingredients that have demonstrated efficacy against F. occidentalis in previous studies include acetamiprid (Assail 30 SG; United Phosphorus, Inc., King of Prussia, Pennsylvania), cyantraniliprole (Exirel; DuPont, Wilmington, Delaware), novaluron (Rimon 0.83 EC; Makhteshim Chemical Works Ltd, Be'er Sheva, Israel), and tolfenpyrad (Apta 1.3 SC; Nichino America, Wilmington, Delaware) (Willmot et al. 2013; Funderburk et al. 2014; Srivastava et al. 2014). These materials were evaluated in rotations with spinetoram. Sulfoxaflor (Closer SC), a new insecticide produced by Dow Agrosciences, was also included. Bifenthrin (Brigade WSB; FMC Corporation, Philadelphia, Pennsylvania) is a pyrethroid insecticide commonly used by Florida strawberry growers as a “clean-up” spray and to control various pests during the growing season. Bifenthrin was tested as a stand-alone material to evaluate the effect of repeated applications of a pyrethroid on numbers and species of thrips.

Spinetoram affects nicotinic/gamma amino butyric acid-gated chloride channels. The other insecticides represent different modes of action. Acetamiprid and sulfoxaflor are nicotinic acetylcholine receptor agonists. Cyantraniliprole is an anthranilic diamide insecticide that kills by disrupting calcium metabolism via the ryanodine receptors. Novaluron is a chitin biosynthesis inhibitor and the only insecticide included without efficacy against adult thrips. Tolfenpyrad is a mitochondrial complex I electron transport inhibitor. Bifenthrin is a sodium channel modulator.

Adult thrips in strawberry flowers were identified to species in order to describe the thrips species complex associated with strawberry in central Florida and to determine how the various insecticide programs affected thrips species. In 2015, adult and 2nd instar thrips on fruit were also tabulated at the species level. In addition, treatment impacts on numbers of Orius predators and on strawberry yield were evaluated.

Materials and Methods

The efficacy of 6 programs of insecticide products were compared with an untreated control for flower thrips control in strawberry at the Gulf Coast Research and Education Center, Wimauma, Florida (27.7599833°N, 82.2241000°W) in the winter-spring of 2013–14 and 2014–15. ‘Strawberry Festival’ transplants were set in the field on 8 Oct 2013 and on 14 Oct 2014 in plastic mulched beds, 33 cm high and 69 cm across the top, and with 1.2 m bed spacing. Overhead irrigation was applied for about 2 wk after setting to aid in establishment of the trans plants. Drip irrigation was used for the remainder of the experiment. Plots were 3.8 m in length and consisted of 20 plants in two 10-plant rows per bed. The study area was treated with fungicides and Bacillus thuringiensis-based products only while waiting for natural populations of flower thrips to build to a level of about 20 or more adults per 10 flowers. Treatment applications began on 11 Mar 2014 and on 10 Feb 2015 and consisted of 4 weekly applications of products (Table 1).

Treatments were replicated 4 times in a randomized complete block design and were applied using a hand-held sprayer with a spray wand outfitted with a nozzle containing a 45° core and a number 4 disc. The sprayer was pressurized by CO₂ to 40 psi and calibrated to deliver 934 L/ha (100 gallons/acre). Samples were collected before treatment applications began and then weekly, 2 d after a treatment application, and consisted of 10 open flowers per plot, placed in vials of 70% isopropyl alcohol that were agitated to dislodge thrips from the plant material. In 2015, 5 green and 5 pink fruits per plot were also sampled similarly to the flowers. Data were recorded initially as adult or larval thrips and Orius spp. per 10 flowers. All specimens of adult thrips were retained, slide mounted, and identified to species. Second instar larvae collected from fruit were also slide mounted and identified to species. Data were transformed by log₁₀ (x + 1) before ANOVA using a factorial model statement with experiment-year and chemical rotations as factors. Means were separated by Tukey's studentized range test (α = 0.05) (SAS Software 2008). Means are reported in the original scale. Yield data were collected once a week for 5 wk each year.

Results

In 2014, thrips adults collected from flowers in the control from 5 Mar through 1 Apr consisted of 77.68% F. bispinosa, 7.00% Haplothrips gowdeyi (Franklin) (Phlaeothripidae), 4.86% F. occidentalis, 3.70% Frankliniella schultzei (Trybom) (Thripidae) and 0.06% Scolothrips sp. (Thripidae). Because of damage, 6.70% could not be identified. In 2015, thrips adults collected from flowers in the control from 12 Feb through 4 Mar consisted of 87.09% F. bispinosa, 10.14% F. occidentalis, 1.25% H. gowdeyi, 0.74% Thrips spp., and 0.39% unknown.

Table 1.

Schedule of treatment applications, with chemical names, application rates, trade names and formulations, concentrations of 495 active ingredients (a.i.), and Insecticide Resistance Action Committee (IRAC) mode of action codes of products, used in the 2014 and 496 2015 experiments in Wimauma, Florida.

Season-long response variables were analyzed with year, treatment, and the year by treatment interaction as factors. The effect of treatment was significant each year for numbers of adult thrips (2014: F = 6.50; df = 6,102; P < 0.0001; 2015: F = 6.78; df = 6,102; P < 0.0001) and larval thrips (2014: F = 27.82; df = 6,102; P < 0.0001; 2015: F = 5.29; df = 6,102; P < 0.0001), and for numbers of F. bispinosa (2014: F = 11.06; df = 6,102; P < 0.0001; 2015: F = 6.92; df = 6,102; P < 0.0001) collected from flower samples. The year by treatment interaction for flower samples was significant for total thrips adults (F = 2.48; df = 6,207; P = 0.024), total thrips larvae (F = 11.60; df = 6,207; P < 0.0001), and F. schultzei adults (F = 16.0; df = 6,207; P < 0.0001). The year by treatment interaction was not significant for F. bispinosa (F = 0.85; df = 6,207; P = 0.536) or F. occidentalis adults (F = 1.85; df = 6,207; P = 0.091). Therefore, treatment effects on seasonlong densities of total thrips adults, larvae, and F. schultzei adults will be discussed by year, and treatment effects on F. bispinosa and F. occidentalis adults for 2014 and 2015 will be discussed with years combined.

TOTAL THRIPS ADULTS AND LARVAE IN FLOWER SAMPLES

In 2014, total adult thrips numbers were significantly lower in all spinetoram treatments than in the control, and there were no statistical differences among spinetoram treatments with regard to total adult thrips numbers (Table 2). Numbers of total adult thrips in the bifenthrin treatment (program 7) were not different from the control (program 1) or 3 of the spinetoram treatments (programs 3, 4, and 6). In 2014, densities of larval thrips were significantly higher in the bifenthrin treatment (program 7) than in all other treatments. Also that year, densities of larval thrips were higher in the control (program 1) than in all insecticide rotations except for the tolfenpyrad-sulfoxafloracetamiprid-spinetoram treatment (program 6). In 2015, numbers of total adult thrips and larvae were significantly lower in all insecticide treatments than in the control but did not differ significantly among insecticide treatments.

Table 2.

Mean (± SE) larval and adult thrips densities in flowers, pooled over the 4 sampling dates (each 2 d after application) in the 2014 and 2015 experiments in Wimauma, Florida.

ADULT S OF F. OCCIDENTALIS IN FLOWER SAMPLES (2014–2015 COMBINED ANALYSIS )

Densities of F. occidentalis adults were significantly higher in the bifenthrin treatment (program 7) than in all other treatments, including the control (program 1), except for the spinetoram-acetamipridnovaluron-spinetoram treatment (program 4) (Table 3). Densities of F. occidentalis adults were not significantly different among spinetorambased insecticide rotations (programs 2–6) or the control (program 1) either year.

Table 3.

Mean (± SE) densities of Frankliniella bispinosa and Frankliniella occidentalis adults in flowers, pooled over the 4 sampling dates (each 2 d after application) and over both 2014 and 2015 experiments. Mean (± SE) densities of Frankliniella schultzei adults in flowers, pooled over the 4 sampling dates (each 2 d after application) in each of the 2014 and 2015 experiments in Wimauma, Florida.

ADULT THRIPS ON FRUIT IN 2015

The numbers of adults collected from fruit were low (Table 4). The majority collected were F. bispinosa, F. occidentalis, F. schultzei, and Scirtothrips dorsalis Hood (Thripidae). There were significantly fewer total adult thrips and F. bispinosa adults on fruit in the spinetoramacetamiprid-novaluron-spinetoram (program 4) and bifenthrin (program 7) treatments than in the cyantraniliprole-spinetoram-sulfoxafloracetamiprid treatment (program 5). The numbers of F. occidentalis, F. schultzei, or S. dorsalis adults on fruit did not differ significantly among treatments.

Table 4.

Mean (± SE) densities of adult thrips in pink and green fruits, by combined and individual species, pooled over the 4 sampling dates (each 2 d after application) in the 2015 experiment in Wimauma, Florida.

LARVAL , PREPUPAL , AND PUPAL THRIPS ON FRUIT IN 2015

Larvae were more numerous than adults on fruit. The majority of 2nd instar larvae were F. bispinosa (Table 5). There were significantly fewer 1st instar, 2nd instar, and total larvae on fruit in the bifenthrin treatment (program 7) than in the control. Second instar larvae were significantly less abundant in all spinetoram rotations than in the control, but there were no significant differences in abundance of 1st instars between the spinetoram treatments and the control. There were significantly fewer total larvae on fruit in the spinetoram-spinetoramsulfoxaflor-spinetoram (program 2) and the spinetoram-acetamipridnovaluron-spinetoram (program 4) treatments than in the control (program 1).

Table 5.

Mean (± SE) larval thrips densities in pink and green fruits, by combined and individual species, pooled over the 4 sampling dates (each 2 d after application) in the 2015 experiment in Wimauma, Florida.

Numbers of 2nd instar F. occidentalis, F. schultzei, and S. dorsalis larvae were low in the control (0.1 ± 0.1 per 10 fruit), and they did not attain high densities in most treatments during the 4 wk of sampling. Numbers of 2nd instar F. occidentalis larvae were higher in the tolfenpyrad-sulfoxaflor-acetamiprid-spinetoram treatment (program 6) than in the spinetoram-acetamiprid-novaluron-spinetoram (program 4) and the cyantraniliprole-spinetoram-sulfoxaflor-acetamiprid (program 5) treatments; however, densities of F. occidentalis larvae were probably not economically significant on fruit even at their most abundant. There were no significant differences among treatments with regard to numbers of 2nd instar larvae of F. schultzei and S. dorsalis on fruit.

Low levels of thrips prepupae and pupae were collected on green and pink fruit, usually on the portion of the fruit in contact with the plastic mulch. The numbers of prepupae and pupae, which collectively averaged less than 1 quiescent stage per 10 fruit, did not differ significantly among treatments (F = 0.77; df = 6,102; P = 0.593).

Discussion

Frankliniella bispinosa was the predominant species collected in flowers each season and on fruit in 2015. Low numbers of F. occidentalis, F. schultzei, H. gowdeyi, and other species were also collected each season. Frankliniella schultzei was first detected in south Florida in 1997 (Frantz & Fasulo 1997). Like F. bispinosa and F. occidentalis, F. schultzei has a broad host range and is a pest of concern in several crops because it transmits tospoviruses (Kakkar et al. 2012; Webster et al. 2015). Haplothrips gowdeyi is a flower feeder and not considered to be of economic importance (Childers & Nakahara 2006).

Season-long densities of F. bispinosa populations were reduced equally by all insecticide rotations each season regardless of the number of spinetoram applications. This indicates that F. bispinosa is broadly susceptible to a range of modes of action, including spinetoram. By contrast, season-long densities of F. occidentalis populations were unaffected by insecticide rotation applications, regardless of the number of spinetoram applications. Lack of treatment effects on F. occidentalis may have been influenced by the low numbers of F. occidentalis in this study. However, these results indicate a lack of susceptibility of F. occidentalis not just to spinetoram but also to products with other modes of action.

Repeated applications of bifenthrin reduced F. bispinosa populations to levels significantly lower than those found with spinetorambased rotations. However, the abundance of F. occidentalis was actually increased relative to other treatments, including the untreated control, by repeated applications of bifenthrin. This may be explained by release of F. occidentalis from both competition with F. bispinosa and predation by Orius (Funderburk et al. 2015), because no Orius were recovered from the bifenthrin treatment in either year. Reitz et al. (2003) found that applications of esfenvalerate and acephate reduced numbers of Frankliniella tritici (Fitch) and F. bispinosa in field pepper but increased numbers of F. occidentalis. Numbers of total thrips larvae and F. schultzei adults were also significantly higher in the bifenthrin treatment in 2014 but not in 2015.

Frankliniella bispinosa is clearly the most abundant thrips species on strawberries in Florida's major strawberry-producing region, but it is also more susceptible to insecticidal control than F. occidentalis. Our results suggest that as insecticide applications are made during the course of the season, populations of F. bispinosa will be reduced and F. occidentalis may become more abundant. Thus, thrips damage to strawberries may be due to the species that is least susceptible to control rather than the species that is most abundant early in the cropping season. However, the relative importance of various stages or species has yet to be critically determined.

The reason that thrips populations reached uncontrollable levels in the spring of 2013 remains uncertain; however, it is possible that environmental factors contributed to the population build-up. Frankliniella bispinosa has many cultivated and wild hosts in central Florida, including perennial hosts such as citrus and oak (Fagales: Fagaceae) (Frantz & Mellinger 1990; Childers & Nakahara 2006). Spring was unusually cool in 2013. Wild hosts such as Raphanus raphanistrum L. (Brassicales: Brassicaceae) continued to flower abundantly, providing resources to F. bispinosa later into the spring than is usual. Samples of strawberry and other infested plants brought to the diagnostic clinic at the Gulf Coast Research and Education Center in the spring of 2013 contained primarily adult thrips, which suggests the infestations may have been the result of large migrations of thrips from wild hosts into cultivated fields.

Historically, thrips have been a sporadic pest in Florida strawberry (Whidden 2004, 2008). The intensive harvest schedule for the crop reduces opportunities for thrips to damage ripened fruit. Spider mites (Tetranychus species; Acari: Prostigmata: Tetranychidae) and armyworms (Spodoptera species; Lepidoptera: Noctuidae) are habitual pests of strawberry, and growers apply insecticides routinely to control them. Spotted wing drosophila (Drosophila suzukii [Matsumura]; Diptera: Drosophilidae) has recently become established as a pest of strawberry and other crops in Florida. When broad-spectrum insecticides such as pyrethroids are sprayed to control these primary pests, a species shift toward F. occidentalis may occur. Presumably, thrips damage occurs 1) when high numbers of adults migrate from neighboring habitat (i.e., wild hosts or end-of-season crops that are being destroyed); 2) when lapses in monitoring allow thrips to build up and feed on green and pink fruit; or 3) when insecticide sprays reduce natural enemies such as Orius and shift the population so that insecticide-tolerant individuals predominate.