Light spectra blocking films reduce numbers of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae) in strawberry, Fragaria x ananassa

Frankliniella occidentalis is a pest of horticultural crops, including commercial strawberry (Fragaria x ananassa). Control is challenging because certain populations are resistant to insecticides and, in strawberry, now relies on the application of biocontrols. However, this approach is not always successful if F. occidentalis populations overwhelm biocontrols. We investigated whether targeted spectral modifications to cladding materials could reduce numbers of F. occidentalis, in strawberry flowers. Five UV‐attenuating plastic‐film materials were tested in three, 6‐week, semi‐field tunnel experiments containing strawberry plants. F. occidentalis were introduced into tunnels from a laboratory culture and subsequent numbers that developed in strawberry flowers were recorded. Limiting UV‐A radiation to the crop significantly reduced the numbers of adult and larval F. occidentalis in strawberry flowers. The numbers of adult (and larvae) in flowers were reduced by 42 (47)%, 54 (41)%, 70 (73)%, and 82 (73)% in UV350, UV370, UV400, and UV430‐attenuating films, respectively, compared with the UVopen (control) film. However, no damage to strawberry fruits was observed regardless of the film treatment. Incorporating UV‐attenuating films as tunnel cladding can suppress F. occidentalis numbers in strawberry. Reducing populations of F. occidentalis in crops is likely to enable the more successful use of other non‐chemical control strategies.

Frankliniella occidentalis is a prevalent pest of cultivated strawberry (Fragaria x ananassa). All stages of strawberry flower and fruit are susceptible to thrips feeding, although larvae are more damaging than adults (Sampson, 2014). Feeding damage can cause malformed smaller fruits, reduction in yields, and bronzing of the fruit surface reducing marketable yield (Nondillo et al., 2010). At the flowering stage, feeding damage to the stamens and floral receptacle is observed (Nondillo et al., 2010) and petals can become russetted and wither early. Strzyzewski et al. (2021) reported that two adult F. occidentalis females per flower caused a decrease in fruit set and increased distortion (commonly known as 'cat-facing') on the developing fruitlets. However, this impact is cultivar and growing condition dependent (pers. obs.) and can be confounded with interactions with other insect pests, such as mirids (Easterbrook, 2000;Rahman et al., 2010). Feeding on small, green fruit reduces the size of mature fruit (Strzyzewski et al., 2021) and bronzing is often observed under the fruit calyx and around the achenes (Nondillo et al., 2010). In a study with 20 caged F. occidentalis adults on strawberry plants for 5 days, 17.6% of the fruits were bronzed, with more than 40% of the fruit surface displaying bronzing damage (Nondillo et al., 2010).
Frankliniella occidentalis is adapted to warm conditions, becoming active particularly early on forced (early flower initiation) tunnelgrown strawberries clad with insulating materials (Sampson, 2014).
The optimum temperature for development of F. occidentalis on strawberry plants is 25 C (Nondillo et al., 2008;Robb, 1989;van Rijn et al., 1995), where the time from egg to egg can occur in only 15.2 days (Robb, 1989). At temperatures higher than 25 C, adult thrips survival is decreased (Malais & Ravensberg, 2004). In addition, F. occidentalis invade crops throughout the growing season from a wide host range including annual flowering weeds (Sampson et al., 2021).
Applications of entomopathogenic fungi can also be employed to target the pupal stage in the soil (Lee et al., 2017). However, entomopathogenic fungi are not commonly used for F. occidentalis control in polytunnel-grown crops as they do not give adequate control, potentially because humidity is too low or thrips do not come into contact with enough spores. In addition, arthropod biocontrol solutions can fail when F. occidentalis becomes too numerous in the crop (pers. obs.).
Frankliniella occidentalis is attracted to blue-coloured surfaces (Broughton & Harrison, 2012;Díaz et al., 2006;Doukas & Payne, 2007;Johansen et al., 2018), and this is exploited for mass trapping. In semi-protected strawberry crops, mass trapping with blue sticky roller traps reduced adult thrips numbers by 61% in flowers, and fruit bronzing by 55%, compared with an untreated control.
Follow on studies where the F. occidentalis aggregation pheromone, neryl (S)-2-methylbutanoate, was added to traps, doubled the trap catch (Sampson, 2014;Sampson & Kirk, 2013). However, the type of glue used can also influence F. occidentalis attraction to traps and interfere with colour perception (Van Tol et al., 2021).
More often control approaches are combined to target different life stages of F. occidentalis for season-long management (Cloyd, 2019), as a single approach is not adequate to reduce crop damage below economic thresholds . While many approaches are highly effective at low pest pressure (Saito & Brownbridge, 2018), under optimal conditions for the pest, F. occidentalis populations can increase too rapidly for biologicals to keep the pest in check. An approach that suppresses thrips rapid population build-up would enhance other methods of control.
The potential for suppressing F. occidentalis populations by disrupting visual perception through the interference of available light has been reviewed by Fennell et al. (2019). In choice tests, F. occidentalis was more likely to enter chambers clad in UV (ultraviolet) transparent materials compared with chambers fitted with UVattenuating materials (Kigathi & Poehling, 2012), and thrips appeared to fly towards areas where UV was present (Fennell et al., 2019). In addition, UV attenuation reduces the dispersal of F. occidentalis (Kigathi & Poehling, 2012). However, contrary to those findings, thrips show a reduced preference for tunnels with high UV-B (Mazza et al., 1999), indicating that their responses to light may depend on the predominant behaviour, for example, feeding or dispersing (Fennell et al., 2019).
As part of a study to test if UV-attenuating tunnel films suppressed Drosophila suzukii Matsumura in strawberry fruits (Fountain et al., 2020), we aimed to investigate whether the same innovative materials would reduce F. occidentalis numbers in the same crop, hence giving a dual pest control benefit. The aim of this study was to investigate if UV-radiation attenuating plastic-film materials over strawberry crops could reduce the numbers of F. occidentalis in strawberry flowers, and what level of UV attenuation is required to do this. There were three experiments, one in each year, which ran for 6 weeks each. Both clear and diffuse films (scatter inbound radiation) were used in 2016 with two UV light transmission films (UVopen and UV350). As diffuse films did not impact pest numbers, the following year, four clear films were tested (UVopen, UV350, UV370, and UV400). There were three replicates of each treatment (Table 1). In the final experiment (2018), the replicates were increased to eight to improve statistical power. The 12 tunnels were divided with fine mesh (Plain Leaded Net Curtain Fabric; Dunelm Ltd., Syston, Leicestershire, UK) into two compartments (12 m 2 ). Three films were compared: UVopen, UV370, and UV430 (Lumitec) ( Table 1).

F. occidentalis rearing and colony maintenance
Light transmission of the films was measured from 300 to 2500 nm at 2 nm steps using an Agilent Cary 7000 Universal Mea-   F I G U R E 1 Spectral transmission (%) versus wavelength (nm) for all cladding films (UVopen (control), UV350, UV370, and UV400 and UV430 (Lumitec)) measured by Cary 7000-diffuse using reflectance accessories (first published in scientific reports Fountain et al., 2020) and 2017) or two rows (2018). In 2018, both cultivars were in all tunnels (10 bags of each, side-by-side in a row Biosystems GmbH, Nussloch, Germany).
We originally intended to record damage to strawberry fruits (bronzing/russeting), but the damage in all 3 years was insignificant and hence not analysable.

DISCUSSION
We demonstrated, for the first time in strawberry, that attenuation of ultraviolet radiation (Figure 1) via spectral filters in polytunnel film materials could significantly reduce the numbers of adult and larval F. occidentalis in strawberry flowers. This is a significant finding that could also enable better incorporation and success of other nonchemical approaches to thrips control, which ordinarily work at low F. occidentalis numbers (e.g., biocontrol agents including predatory mites and Orius).
We did not observe enough thrips feeding damage to assess in this study, which we attribute to fewer than four thrips per flower (Sampson, 2014). Reportedly, two adult F. occidentalis females can cause cat-facing on the developing fruitlets (Strzyzewski et al., 2021).
However, in our experience, this is more typical of mirid feeding and far more thrips per flower are needed to cause bronzing on strawberry fruits. Indeed, 20 adult thrips were needed to cause 40% surface bronzing of 17.6% of fruits in a study by Nondillo et al. (2010). However, our results indicate that suppressing F. occidentalis numbers in strawberry flowers might reduce fruit damage in higher populations.
By limiting the levels of UV able to reach the crop, where F. occidentalis were introduced, the number of adult (and larval) F. occidentalis per strawberry flower was reduced by 42 (47)%, 54 (41)%, 70 (73)%, and 82 (73)% for UV350, UV370, UV400, and UV430 (Lumitec) films respectively, compared with the UVopen control film. A significant reduction in adults and larvae was observed for films that attenuated light below 430, 400, or 370 nm, with the lowest number of adults and larvae found under the UV400 and UV430 films. The UV350 film, which attenuated light from 350 nm and below, did not significantly reduce pest numbers. It is notable that the films do not block spectra linearly (Figure 1). Indeed, the film blocking below 400 nm has an additional transmission peak at around 310 nm. However, overall, the general trend was that the higher the spectral wavelength attenuation, the fewer F. occidentalis were found in strawberry flowers.
Spectral balance is important in insect pest navigation, flight orientation, and food sourcing. Thrips (Thysanoptera) generally have a very restricted range of perception within the UVA (300-400), violetblue (401-500), and green-yellow (501-560) spectra compared with other insect orders (Fennell et al., 2019;Liu et al., 2019;Matteson et al., 1992). UV is an important cue for take-off flight of thrips F I G U R E 2 Overall, mean (AES.E) numbers of adult (left) and larval (right) Frankliniella occidentalis per strawberry flower from tunnels clad with UV-attenuating films compared with a UV open control across all timepoints; combined data from all three field experiments (2016,2017,2018). Different letters denote significant differences in thrips numbers between films (Tukey's HSD, α = 0.05) (Mazza et al., 2010); however, it is not clear how the attenuating film in our study affected F. occidentalis behaviour. In addition, light intensity can change the response of thrips to spectral wavelengths, as demonstrated in Liu et al. (2019). In our study, potentially constricting the spectral range may reduce flower reflection and hence recognition by the thrips and attraction to flowers, preventing dispersal to new egg-laying sites, but more research is needed to demonstrate this.
Thrips seeking a food source may seek locations with increased green reflectance or reduced UV, whereas those in dispersal phases are attracted to areas with higher UV spectra (Fennell et al., 2019;Mazza et al., 1999). However, thrips attraction to host plants tends to be in the green spectral range at over 500 nm (R} oth et al., 2016) and hence would not be expected to be influenced by these films. Also, at 500 nm, the Lumitec film had a transmission of around 60%, so that green plants may have appeared darker and less clear than usual.
Alternatively, F. occidentalis in our study may have moved away from the strawberry flowers under the light attenuating films. Fennell et al. (2019) concluded that the main mechanisms of suppression of insect pests by films were (i) positive phototaxis to ultraviolet light sources, and (ii) reduced take-off and flight behaviour when UV was absent, indicating that UV is probably acting as a cue for open sky during take-off and for orientation once in flight (Cronin & Bok, 2016). Suppression of thrips was attributed to both a reduction in pest immigration into the crop, and within crop movement (Fennell et al., 2019), although F. occidentalis reportedly moves less than 30 cm per day from release points (Rhainds & Shipp, 2004), and is a relatively a weak flyer  relying on dispersal by wind for longdistance transport (Mound, 1983;Nyasani et al., 2017). Hence, in our study, a combination of factors may have been at play, including movement away from plants and non-recognition of egg-laying sites.
Both of which would result in fewer F. occidentalis larvae and a reduction in population growth. Clearly, more studies are needed to establish the true mechanism of how UV-attenuating films influence F. occidentalis behaviour and subsequent populations.
In addition to reducing the numbers of F. occidentalis in strawberry films, the UV-attenuating films used in this study also reduced egg laying by D. suzukii in strawberry fruit in the same experiment (Fountain et al., 2020). Adult D. suzukii emergence from strawberry fruit (a proxy for egg laying) was reduced up to 8%, 22%, 34%, and 73% for UV350, UV370, UV400, and UV430 films, respectively, compared with the UVopen cladding. This offers added benefit to fruit growers through the suppression of two key strawberry pests simultaneously. It is not anticipated that there would be a significant interaction between D. suzukii and F. occidentalis in this study as the former oviposits in ripening and ripe fruits, and the latter generally inhabits the flowers and early fruitlets. Our approach using UV-attenuating films significantly reduced F. occidentalis numbers in strawberry, enabling other methods that work more effectively at low populations to be combined with more success (e.g., biocontrols). If the same effect, as reported in this study, when thrips numbers were low were to be found at higher thrips population densities, then this would have the effect of reducing thrips damage and crop losses.   (Blumthal et al., 2005). Light-emitting diodes (LEDs) are a promising approach to increase the attractiveness of visual traps, for example, blue LEDs could be used to enhance the capture of mass traps in the 'pull' approach (Johansen et al., 2018;Otieno et al., 2018;Stukenberg et al., 2020). It is likely that attractant strategies would vary depending on the target crop and time in the season (Johansen et al., 2018).
Most of our films (except the control) blocked UV-C, UV-B, and UV-A (Lumitech) to some degree. UV-C can be used as a treatment for powdery mildew, Rhizopus and Botrytis pathogens of strawberry (Forges et al., 2020), and UV-B has future potential application for control of plant diseases but is also important in plant responses such as flowering initiation and photosynthesis (Meyer et al., 2021). Indeed, UV transmitting films are demonstrated to reduce powdery mildew in strawberry (Onofre et al., 2022), hence any benefits from pest reduction (Fountain et al., 2020 and this study) need to be balanced with losses in production caused by plant pathogens.
Finally, our films were tested in 12 m flight cages with 1 Â 1 mm insect exclusion mesh on strawberry. To fully test these films, they should be trialled on commercial farms on a range of crops in different geographical regions and incorporated as part of an integrated pest and disease management strategy.

AUTHOR CONTRIBUTIONS
Michelle T. Fountain conceptualized the study. Alvaro Delgado and Sebastian Hemer tested increasing UV-attenuating in protective field claddings. Greg Deakin advised on experimental design and statistics and Frederick Davis supplied the data on film transmission (Figure 1).
Michelle T. Fountain and Sebastian Hemer prepared the manuscript.

ACKNOWLEDGMENTS
This work was funded by the Innovate UK project 102526. We thank British Polythene Industries for supply of the greenhouse materials and co-sponsoring the research. We are grateful to the NIAB East Malling farm manager Graham Caspell and his field staff for support and Berry Gardens agronomists for advising on the husbandry of the strawberry plants.

DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.