1. Introduction
Thrips tabaci Lindeman (Thysanoptera: Thripidae) is one of the most economically important insect pests of onion (
Allium cepa L.) worldwide [
1,
2]. Adults and larvae feed on leaves causing a reduction in photosynthetic production, typically leading to smaller bulb sizes [
3]. Feeding injury to onion leaf tissue creates entryways for bacterial and foliar pathogens, which also can be spread among plants by adults [
4,
5,
6,
7]. Thrips also vector Iris yellow spot virus (family Bunyaviradae,
Tospovirus spp. (IYSV)), which can kill onion plants before they fully mature as well as reduce bulb sizes [
8,
9,
10].
Management of
T. tabaci on onion relies on the use of insecticides in both conventional and organic production systems. Although resistance in
T. tabaci populations has not been documented to the most commonly used insecticide, spinetoram [
11], resistance to pyrethroids and organophosphates has been documented in New York, USA [
12,
13] and Ontario, Canada [
14] and resistance to methomyl and oxamyl (carbamates) and abamectin (Avermectins, Milbemycins) in the Pacific Northwest, USA [
15]. Unlike conventional onion production where many insecticides in several different Insecticide Resistance Action Committee (IRAC) classes are available [
1,
2], organic growers have fewer products allowable by the USDA Standard Organic Practices guidelines [
16]. The need for non-chemical strategies for managing
T. tabaci is crucial to reduce the risk of resistance developing in organic onion production due to repeated use of a limited number of effective active substances. Additionally, non-chemical strategies also can help minimize adverse side effects of pesticides on non-target beneficial organisms, human health, and the environment.
Plastic mulches are used in vegetable production for weed suppression [
17,
18], soil moisture retention [
19,
20], reduced soil erosion, modulation of soil temperatures [
21,
22], and pest management [
23,
24]. Ultraviolet (UV) reflective mulches have become popular in the production of various crops for their ability to reduce insect pest pressure [
25,
26,
27,
28], including thrips. Because thrips locate their host plants in part by using visual cues in the UV spectrum, UV-reflective plastic mulches may obscure host location cues used by thrips [
29]. UV reflective silver mulch reduced populations of
Frankliniella occidentalis (Pergande),
F. tritici, and
F. bispinosa in tomato [
30] and
F. occidentalis and
T. palmi in pepper [
31,
32]. Less is known about the effect of UV-reflective silver mulches on
T. tabaci in onion. In two previous studies, silver reflective mulches reduced numbers of
T. tabaci in onion early in the season with differences fading as the season progressed [
33,
34].
Thrips tabaci has shown affinity toward certain types of onion phenotypes. Phenotypes with blue-gray, “waxy” leaves tend to be more attractive and support higher densities of
T. tabaci and have more feeding damage compared with those that have lighter-green (“glossy” or “semi-glossy”) leaves [
35,
36,
37,
38]. The natural variation of amounts and types of epicuticular waxes on leaves is responsible for these visual differences, and a higher amount of the ketone hentriacontanone-16 (H-16) relative to the other waxes is associated with greater feeding damage [
39,
40]. Glossy phenotypes have much lower amounts of H-16 compared to waxy onion phenotypes [
37]. While low levels of H-16 are beneficial for reducing thrips colonization and their damage, these onion phenotypes tend to be more susceptible to spray damage, foliar pathogens, and excessive transpiration [
41]. Onion phenotypes with “semi-glossy” leaves tend to have higher amounts of H-16 than glossy phenotypes, but also higher amounts of other epicuticular waxes. Consequently, some semi-glossy phenotypes may have a similar amount of total waxes as waxy phenotypes, which would provide more protection of the leaves against spray damage and foliar pathogens, but also benefit in being less attractive to and damaged by thrips. Field studies in conventional onion fields in New York have shown that semi-glossy onion cultivars can provide some protection against
T. tabaci, although increased bacterial disease incidence also occurred [
42,
43,
44]. Similar semi-glossy onion cultivars have not been evaluated in organic production systems.
Organic farms that are certified by the United States Department of Agriculture (USDA) must adhere to strict rules regarding production, food safety, and pest management [
16]. Many biopesticides fall within these regulations and must be approved by the Organic Materials Review Institute (OMRI) or the Washington State Department of Agriculture (WSDA) Organic Food Program. Spinosad (Entrust
®, Corteva Agriscience, Indianapolis, IN, USA), produced from a soil-inhabiting actinomycete bacterium,
Saccharapolyspora spinosa [
45], is one of the most commonly used biopesticides for managing insect pests in organic vegetable production and is effective against several onion insect pests [
46,
47,
48]. Spinetoram (Radiant
®, Corteva Agriscience, Indianapolis, IN, USA), spinosad’s conventional counterpart, is arguably one of the most effective active ingredients for managing
T. tabaci in conventional onion production throughout the northern US [
1,
2,
49]. Few other OMRI-listed biopesticides have shown promise for reducing
T. tabaci densities in onion [
48,
50,
51,
52].
An integrated approach for managing T. tabaci in onion is crucial due to the lack of available active ingredients that successfully reduce T. tabaci populations and the development of insecticide resistance in organic production systems. The objective of our study was to evaluate combinations of UV-reflective mulch and semi-glossy onion cultivars, with and without biopesticides, to determine the most effective integrated management approach for T. tabaci in organic onion production. We hypothesized that each management tactic would provide some reduction in thrips densities, but that the most effective strategy would be a combination of UV-reflective mulch, semi-glossy cultivars, and biopesticide applications. We also hypothesized that bulb yield would be greatest following strategies that were most effective against T. tabaci.
4. Discussion
Few IPM programs in organic onions include multiple tactics for managing a single insect pest. For example, T. tabaci is managed nearly exclusively with insecticides in organic systems. Because insecticides that effectively reduce populations of T. tabaci are limited and the potential for insecticide resistance is high in organic production systems, an integrated approach using a combination of non-chemical and chemical strategies is crucial for T. tabaci management. Thus, in this study, we examined a multipronged approach to determine the most effective combination of integrated management tactics for T. tabaci in onion. We hypothesized that reflective mulch combined with a semi-glossy cultivar and a biopesticide program would maximize onion thrips control. We also hypothesized that bulb yield would be greatest following management strategies that were most effective against T. tabaci. While a combination of the semi-glossy cultivar “Rossa di Milano” and the biopesticide treatment spinosad + neem oil significantly reduced thrips densities, reflective mulch had little impact on thrips densities. Despite improving T. tabaci management using a combination of “Rossa di Milano” and the biopesticide treatment, total yield and the proportion of large bulbs in this treatment were lower than those in the thrips-susceptible “Bradley” treated with the biopesticide treatment. Similarly, T. tabaci densities and marketable yield in the semi-glossy cultivar B5336AxB5351C combined with the biopesticide treatment were comparable to those in the “Bradley” and biopesticide treatment combination. The benefits of reducing T. tabaci densities using reflective mulch were slight and inconsistent. However, when reflective mulch was combined with the biopesticide treatment, yields were higher than in the treatment combining white mulch and the biopesticide treatment, regardless of cultivar. Our study highlights the complexity of selecting a combination of IPM tactics that effectively manage T. tabaci, while also optimizing yield.
Biopesticide use was the most effective tactic for managing
T. tabaci in our study. Onions sprayed with spinosad + neem oil had fewer
T. tabaci and produced higher yields than onions that were unsprayed, regardless of mulch type or onion cultivar. Previous studies in onion production regions of the United States and Pakistan have shown that biopesticides are effective for reducing
T. tabaci densities in onion [
47,
57,
58,
59,
60]. However, efficacy depends on the biopesticide applied. Spinosad was the most effective biopesticide for reducing
T. tabaci densities and improving bulb yield in New York and Wisconsin [
46,
47,
48,
55]. Several botanical extracts also have been evaluated for
T. tabaci control in onions. Azadirachtin, derived from the neem tree seeds or leaves (
Azadirachta indica Juss), provided moderate reductions in
T. tabaci densities in studies conducted in the Pakistan [
58,
60] and feeding damage in studies conducted in New York, United States [
48], but improvements in yield were inconsistent. In studies conducted in Ethiopia and Pakistan, Fitiwy et al. [
60] and Khaliq et al. [
58], respectively, reported reductions in thrips densities of 17.2% and >60% using extracts of
Datura spp., respectively. Khaliq et al. [
58] also found a significant reduction of
T. tabaci using tree tobacco (
Nicotinia glauca Graham), as well as a similar yield to the pyrethroid synthetic insecticide lambda-cyhalothrin. Additionally, some of the botanical extracts may be more available and affordable in parts of the world where onions are grown, such as the United States and Canada [
60]. Regardless of onion production region, future research should focus on identifying effective rotations of biopesticide products and using action thresholds to reduce potential insecticide resistance.
Leaf phenotype shows some promise as an approach for managing
T. tabaci in onion. In our study, “Rossa di Milano” had relatively consistent reductions in both adult and larval thrips populations, but this was not evident for B5336AxB5351C. Previous studies indicated that thrips prefer onion cultivars with higher levels of certain epicuticular waxes [
1,
3,
37,
39,
61]. Higher levels of epicuticular waxes are associated with the thrips-susceptible “Bradley”, whereas “Rossa di Milano” and B5336AxB5351C have characteristically lower wax levels. Cultivars with lower amounts of total wax or H-16 have lower densities of
T. tabaci and reduced thrips feeding damage [
37,
38]. The results of our study with “Rossa di Milano” were consistent with these findings. However, the level of thrips damage on cultivars with unique wax profiles can vary based on the number of leaves, time to maturity, and leaf structure (open vs. closed neck), as well as amounts of waxes [
3,
62], which could explain the disparate results we found between “Rossa di Milano” and B5336AxB5351C.
Semi-glossy cultivars must have additional properties that make them acceptable replacements for thrips-susceptible cultivars. “Rossa di Milano” consistently had lower thrips densities, but also had lower marketable total yield than “Bradley”. One potential reason for the lower yield in “Rossa di Milano” is that it simply has a lower yield potential than “Bradley” and such a comparison is not meaningful. The replacement of “Bradley” with a lower yielding thrips-resistant cultivar is not likely to be adopted by onion growers unless fewer insecticide applications are required to protect it against
T. tabaci. Ideally, resistant cultivars should reduce onion thrips densities below action thresholds, thereby reducing the number of insecticide applications applied throughout the season [
42,
49]. In our studies, the mean season densities of onion thrips larvae in the semi-glossy cultivars were above 3 larvae/leaf in 2018 and above 10 larvae/leaf in 2019. An economic injury level (EIL) has been reported as a season mean of 2.2 thrips/leaf in conventionally produced onion [
63,
64], but no EILs have been generated for organic onions. If using a similar EIL, the semi-glossy cultivars in our study would not have been effective enough to withstand
T. tabaci infestations without the use of biopesticides.
Reflective mulch was not a highly effective cultural management tactic for
T. tabaci in our study. Reflective mulch showed an inconsistent reduction of adults and larval populations on certain sampling dates throughout both seasons. This result is in contrast to our hypothesis that reflective mulch would significantly delay thrips infestations by reducing thrips colonization early in the season. Because silver reflective mulch works by reflecting shortwave ultraviolet (UV) wavelengths of sunlight, which confuses and repels incoming adults [
29], we expected that the effect of the reflective mulch would be most prominent in the early season before the onion plant canopy grew large enough to minimize the reflection. We observed reductions in thrips densities on certain dates in both years, but the largest and most consistent reduction in the early season was only seen in 2019, when adult and larval thrips densities were 2–3 times lower than in the white mulch, suggesting that the benefits of reflective mulch may be most evident during hot dry years when
T. tabaci pressure is highest. Although reflective mulches have been used successfully to reduce other insect pest densities including thrips [
25,
28,
31], research on
T. tabaci has been limited and the results are inconsistent. While van Toor et al. [
34] saw no significant differences in
T. tabaci densities among UV-reflective or silver reflective mulches compared with bare ground, Lu et al. [
33] found that reflective mulches were effective at reducing numbers of adult
T. tabaci when shallots were spaced further apart. This result is consistent with the hypothesis that as the plant canopy shades the reflective mulch, the mulch becomes less effective. Even when combined with other IPM tactics, reflective mulch had little effect on reducing
T. tabaci densities in our study.
Reflective mulches provide other benefits to vegetable growers. Silver mulches have improved yields of squash [
25], peppers [
28], and tomatoes [
30]. Hoepting et al. [
65] reported an increase in marketable onion yield that was almost three times greater than that of marketable yield from onions grown on black plastic mulch. In our study, reflective mulch did not improve marketable yield or the proportion of large bulbs compared with those grown on white mulch. Reflective mulches can also reduce pathogen incidence. Hoepting et al. [
65] found that silver mulches reduced bacterial bulb rots 59–75% in onions compared with those grown on bare ground in New York and Pennsylvania. Nyoike et al. [
26] saw a reduction in Cucumber Leaf Crumple Virus (CuLCrV) transmitted by the silverleaf whitefly (
Bemesia tabaci (Gennadius)) in zucchini squash with the use of silver reflective mulch compared to bare ground. Incidence of Tomato Spotted Wilt Virus (TSWV) vectored by
Frankliniella spp. was reduced in tomatoes planted in reflective mulch compared to black mulch [
30]. Although reflective mulches may not consistently reduce
T. tabaci infestations or improve onion yield in New York, there is a possibility that they may reduce Iris Yellow Spot Virus (IYSV), which is transmitted by
T. tabaci and can be an economically devastating problem in many onion-producing regions in the United States [
10,
66].
As far as identifying an optimal combination of IPM tactics for managing T. tabaci in organic onion production, the results from our study failed to show consistent and significant benefits of non-chemical tactics. The application of a tank mix of spinosad + neem oil was highly effective and consistent for T. tabaci management. Further research on relevant economic injury levels for T. tabaci in organic onion production is a necessary first step for measuring the effect of some of the evaluated cultural strategies. For example, the small reduction we saw in thrips numbers in onion grown in reflective mulch may not have translated to improved yield, but any reduction in the number of biopesticide applications during the season is unknown. Additionally, other effective biopesticides are needed for T. tabaci to prevent insecticide resistance in these systems. Action thresholds for spinosad + neem oil are also needed to optimize use of spinosad. Finally, similar research should be conducted in other regions where benefits of multiple IPM tactics, especially non-chemical tactics, may occur.