and Tomato Spotted Wilt Virus - BioOne

HORTICULTURAL ENTOMOLOGY

Reflective Mulch and Acibenzolar-S-methyl Treatments Relative to Thrips (Thysanoptera: Thripidae) and Tomato Spotted Wilt Virus Incidence in Tomato D. G. RILEY,1 S. V. JOSEPH,

AND

R. SRINIVASAN

Department of Entomology, University of Georgia, Tifton Campus, 122 S. Entomology Drive, Tifton, GA 31793

J. Econ. Entomol. 105(4): 1302Ð1310 (2012); DOI: http://dx.doi.org/10.1603/EC11179

ABSTRACT Management of thrips-transmitted tomato spotted wilt (TSW) virus typically relies on tactics that either reduce the thrips vector numbers or change the plantÕs response to the virus to reduce economic loss. We attempted to quantify the interaction between two such tactics, reßective mulch and the plant activator acibenzolar-S-methyl (Actigard), respectively, on a TSW-susceptible tomato hybrid. A split plot experiment was conducted in 2009 and 2010 where main-plots were three types of plastic mulch (two metalized reßective vs. black) and subplots consisted of a range of plant defense activator applications. TSW pressure varied over year with 80% of untreated plants having TSW in 2009 where as ⬍7% of plants was infected in 2010. No signiÞcant interaction between mulch and subplots was found relative to thrips and marketable yield in either year. In 2009, the seasonal average of Frankliniella fusca (Hinds) populations and incidence of TSW were signiÞcantly lower and yield signiÞcantly higher on both reßective mulches than on black mulch. Seasonal averages of thrips and fruit yield differed signiÞcantly among treatments of acibenzolar-S-methyl. However, there was a signiÞcant acibenzolar-S-methyl by mulch interaction relative to TSW incidence. In 2009, a minimum of acibenzolar-S-methyl at transplant plus foliar treatments at 10 and 20 d after transplant was required to signiÞcantly reduce TSW incidence compared with untreated plants before harvest. Under lower TSW pressure in 2010, average TSW incidence was signiÞcantly less in all plots treated with acibenzolar-S-methyl treated plots compared with the check. Acibenzolar-S-methyl treatments functioned better with the thrips reducing tactic, ultraviolet-reßective mulch. We propose that acibenzolar-Smethyl is less effective than metalized reßective mulch in reducing the incidence of TSW in tomato. KEY WORDS Tospovirus, thrip vector, reßective mulch, plant defense activator

Tomato spotted wilt virus (TSWV) (Genus Tospovirus; Family Bunyaviridae) has severely affected tomato production in the United States and worldwide (Goldbach and Peters 1994, Persley et al. 2006). The disease the virus causes, tomato spotted wilt (TSW), has been a major constraint to tomato production in the southeastern United States since the 1980s (Riley and Pappu 2004). In Georgia alone, it is estimated that TSW-induced losses from 1997 through 2006 in tomato, Solanum lycopersicum (L.), and pepper, Capsicum annuum L. crops were approximately $90 million. Losses in peanut and tobacco in Georgia during this time period were estimated to be $236 million (Riley et al. 2011a). This virus is transmitted exclusively by several species of thrips (Thysanoptera) in the family Thripidae (Ullman et al. 1997, Jones 2005). Among the seven thrips species that have been reported to occur in the continental United States and are capable of TSW virus transmission (Riley et al. 2011a), tobacco thrips, Frankliniella fusca (Hinds) and western ßower thrips, Frankliniella occidentalis (Per1

Corresponding author, e-mail: [email protected].

gande) are the major vector species in tomato in Georgia (Riley and Pappu 2000, 2004). Two major control tactics against thrips in tomato are the use of reßective mulches (Greenough et al. 1990, Momol et al. 2004) and insecticide (Momol et al. 2004; Riley and Pappu 2000, 2004). Soil and foliar insecticide treatments applied during early season have been shown to be effective in reducing TSW incidence (Riley and Pappu 2004). Soil applied imidacloprid, which is taken up systemically by the plant, has antifeedant and antisettling effects on F. fusca (Joost and Riley 2005). A new insecticide, cyantraniliprole, which is not yet labeled in fruiting vegetables, has been shown effective against thrips in pepper (Jacobson and Kennedy 2011). Metalized and other ultraviolet (UV)-reßective plastic mulch have consistently reduced thrips and TSW prevalence in the crop (Greenough et al. 1990; Kring and Schuster 1992; Olson et al. 2000; Riley and Pappu 2000, 2004; Diaz et al. 2003, 2007; Reitz et al. 2003; Momol et al. 2004). Management of viral diseases also can be achieved through reducing their impact on the plant through plant resistance. Reducing the TSW incidence in to-

0022-0493/12/1302Ð1310$04.00/0 䉷 2012 Entomological Society of America

August 2012

RILEY ET AL.: THRIPS AND TSWV MANAGEMENT

mato through deployment of TSW-resistant cultivars (Stevens et al. 1992, 2006, Saidi and Warade 2008) has been the mainstay of management of this disease in recent years (Riley et al. 2011b). However, plant resistance to TSW also can be induced in genetically susceptible cultivars of tomato by foliar applications of acibenzolar-S-methyl, a structural analog of salicylic acid that induces natural disease resistance. Momol et al. (2004) demonstrated that such applications are effective in reducing TSW incidence in tomato when applied prior transplant plus every 2 wk for six applications. This treatment is useful when planting TSWsusceptible tomato cultivars which may be grown for other horticultural characteristics. From a research standpoint, this is potentially a very useful tool for establishing different levels of plant response in a TSW-susceptible tomato plant cultigen. Momol et al. (2004), who evaluated an at-plant application followed by biweekly sprays, also suggested it would be useful to evaluate different application schedules of acibenzolar-S-methyl to establish the best use pattern. Different types of UV-reßective mulch and different application timings of acibenzolar-S-methyl to tomato were investigated to quantify their individual and interactive effects on thrips vector control and plant response to TSW. Our hypothesis was that UVreßective mulch would reduce thrips on the plant and incidence of TSW while different use patterns of acibenzolar-S-methyl would not affect thrips but would reduce the incidence of TSW. We suspected that the effects might be additive relative to reducing TSW incidence. This study would also provide some insight into the most effective timing of applications of acibenzolar-S-methyl to prevent TSW incidence on multiple mulch types. This information is important because if resistance to TSW virus falters because of the presence of resistance breaking strains of the virus in tomato (Latham and Jones 1998, Aramburu and Marti 2003, Ciuffo et al. 2005, Gordillo et al. 2008), knowledge of the combined effects of alternate tactics could provide additional protection from TSW. The speciÞc objectives of this study were to determine effects of 1) different types of UV-reßective mulches and 2) different numbers of applications of acibenzolar-S-methyl on TSW incidence, thrips population dynamics, and marketable tomato yield and then to look for interactions between these two control tactics. Materials and Methods Field studies were conducted each spring in 2009 and 2010 at the Coastal Plain Experiment Station, Tifton, GA. The tomato cultivar ÔFL 47⬘ (TSWVÐsusceptible hybrid; Seminis, Saint Louis, MO) free of TSW was transplanted on 16 March and 25 March in 2009 and 2010, respectively, and were spaced 61 cm on a 1.8 m wide bed with 1.5 m wooden stakes between plants. Soil type was a Tift pebbly clay loam soil or sandy loam. All Þeld tests used methyl-bromide fumigated beds at the rate of 224 kg per ha (98:2, Hendrix and Dail, Tifton, GA). A minimum of 560 kg/ha of

1303

10 Ð10-10 fertilizer (Agrium Inc., Denver, CO) was applied to Þeld plots each year and liquid fertilizer (Big Bend Agri-Services Inc., Cairo, GA) 8 kg per ha (7Ð 0-7) was applied every 2 wk with a drip irrigation system. In these tests, tomato plots were treated weekly in April and May with a fungicide (Ridomil Gold-Bravo WP 2.2 kg product/ha; Syngenta, Greensboro, NC) and an insecticide, Bacillus thuriengensis (DiPel 2.2 kg product/ha, Valent U.S.A. Corporation, Walnut Creek, CA) to prevent fungal foliar and root diseases and limit damage induced by commonly occurring lepidopteran insects in tomato without affecting thrips populations. Paraquat (Gramoxone Inteon 2SL 2.31 per ha, Greensboro, NC) was applied to the edges of plastic mulch for weed control. Each year, four replicates of three main treatments, metalized reßective mulches versus black, and Þve subplot treatments, different levels of acibenzolar-Smethyl (Actigard 50 WG, Syngenta Inc.), were evaluated in a randomized split-plot design. The plot lengths of the three main treatments were 18.2 m long plots by six beds with black plastic (1.25 mil, North American Film, Philadelphia, PA), heat-stripe (1.25 mil with a 20 cm wide black stripe down the center and the remaining plastic metalized, Sunup Reßective Films/Star Metal Plating, Inc., Escondido, CA), and solid metalized or UV-reßective (Pliant Corporation, Schaumburg, IL) mulch. This size main plot was deemed necessary to have a signiÞcant effect on thrips numbers in the Þeld (Olson et al. 2000). The width of the top of the plastic beds in the Þeld was 80 cm. Thus, the main plot treatments were 100% black, 25% black ⫹ 75% metalized, and 100% metalized, respectively. The acibenzolar-S-methyl application timings for 30plant subplots were as follows: 1) spray at transplant only, 2) spray at transplant then at 10-d, 3) spray at transplant then 10-d and 20-d, 4) spray at transplant then 10-d, 20-d, and 30-d, and 5) untreated check. Acibenzolar-S-methyl rates 2.3, 2.3, 3.5, and 3.5 mg/m2 were applied at transplant, 10-d, 20-d and 30-d after transplant, respectively. The lower rates on younger plants were used to avoid phytotoxicity effects (Mandal et al. 2008). Tomato plants were monitored for TSW incidence on foliage and fruit (Best 1968, Gitaitis 2009). TSWspeciÞc symptoms were visually evaluated (positive subsample conÞrmed by DAS-ELISA for TSWV) in each plot at weekly intervals beginning 26 March and ending 21 May in 2009. In 2010, weekly evaluations were conducted from 8 April to 9 June. The number of plants with TSW-speciÞc foliar symptoms per plot was recorded throughout at each sampling interval and percent TSW incidence was estimated for each plot. For both years, the number of thrips by species from beat-cup, blossom, and yellow sticky trap samples was determined. Four weekly beat-cup samples followed by four weekly blossom samples were collected from 25 March to 21 May in 2009, and from 8 April to 24 May in 2010, whereas yellow sticky trap samples were collected weekly from 25 to 22 May in 2009, and from 19 March to 28 May in 2010. Beat-cup samples (Joost and

1304 Table 1.

JOURNAL OF ECONOMIC ENTOMOLOGY

Vol. 105, no. 4

Effect of mulch types and acibenzolar-S-methyl on thrips numbers in tomato in 2009, Tifton, GA

Treatment

Mainplot Black mulch Heat-stripe mulch UV-reßective mulch Subplot Acibenzolar-S-methyl at transplant only Acibenzolar-S-methyl at transplant ⫹ 10d Acibenzolar-S-methyl at transplant ⫹ 10d ⫹ 20d Acibenzolar-S-methyl at transplant ⫹ 10d ⫹ 20d ⫹ 30d Untreated check

Beat-cup per 10 plants

Blossom sample per 10 plants

F. fusca

F. occidentalis

F. fusca

F. occidentalis

0.2 ⫾ 0.1a 0.1 ⫾ 0.0a 0.2 ⫾ 0.0a

0.6 ⫾ 0.1a 0.3 ⫾ 0.0a 0.2 ⫾ 0.1a

0.9 ⫾ 0.2a 0.2 ⫾ 0.1b 0.2 ⫾ 0.1b

24.9 ⫾ 2.1a 19.7 ⫾ 1.8a 18.5 ⫾ 2.6a

0.1 ⫾ 0.0a 0.1 ⫾ 0.0a 0.1 ⫾ 0.1a 0.3 ⫾ 0.1a 0.3 ⫾ 0.1a

0.4 ⫾ 0.1a 0.3 ⫾ 0.1a 0.3 ⫾ 0.1a 0.5 ⫾ 0.1a 0.3 ⫾ 0.1a

0.5 ⫾ 0.3a 0.5 ⫾ 0.2a 0.3 ⫾ 0.1a 0.6 ⫾ 0.3a 0.3 ⫾ 0.2a

25.8 ⫾ 3.8a 18.3 ⫾ 1.9a 19.6 ⫾ 3.0a 21.8 ⫾ 1.5a 19.8 ⫾ 3.6a

Yellow sticky trap F. fusca

Total thrips

10.4 ⫾ 1.5a 70.5 ⫾ 3.4a 4.2 ⫾ 0.8b 41.3 ⫾ 9.6b 4.4 ⫾ 0.9b 36.5 ⫾ 3.9b Ñ Ñ Ñ Ñ Ñ

Ñ Ñ Ñ Ñ Ñ

Data were subjected to analysis of variance using generalized linear models. Means in a column within treatment (mainplot or subplot) followed by different letters are signiÞcantly different (P ⬍ 0.05) and were separated using LSD Test.

Riley 2004) involved bending a whole seedling or compound leaf (older plant) into a 946-ml (11.5 cm in diameter, 16.5 cm in depth) Styrofoam cup (Dart Container Corp., Mason, MI) and shaking vigorously for 5 s per plant before collecting thrips off of the cup surface. Beat-cup samples were taken per 10 randomly selected plants per row per week. Blossom samples (Riley and Pappu 2004) consisted of a single tomato blossom in the top third of the plant taken from 10 randomly selected plants per plot and placed into a 20 ml vial containing 10 ml 50% EtOH-water solution. A single cylindrical (2.5 cm diameter ⫻ 7.5 cm) yellow sticky trap for thrips (Cho et al. 1995) was set up in the center of the main plot (mulch treatment) ⬇30 cm above the ground and exposed for a week. Adult thrips trapped by both methods were identiÞed to species using key characteristics (Riley et al. 2010a) from published dichotomous keys (Oetting et al. 1993, Stannard 1968) under 70 Ð140 ⫻ magniÞcation using a SZH10 Olympus (Olympus America, Lake Success, NY) stereomicroscope. Yield was assessed on 8, 15, and 30 June in 2009; and on 3 and 15 June in 2010. Fruit subsamples (up to 48 kg) were harvested from the center six plants per subplot and were graded as small, medium, large, and extra large using USDA standards for fresh market tomato (Sargent and Moretti 2004). Direct thrips feeding damage (dimpling) (Olson 2009), Lepidopteradamaged fruit, physiological fruit damage, blotchycolored fruit, and blossom end rot resulted in fruit being counted as unmarketable. Analysis of variance (ANOVA) using the generalized linear model (GLM) procedure in SAS (SAS Institute 2008) was used to evaluate the effects of mainplot and subplot treatments on percentage TSW incidence, thrips captures, and tomato-fruit yield. The main effect, mulch type was tested using mulch ⫻ replication as error term at ␣ ⫽ 0.05 to explain the variance among subplots as well as between mulch types. Least signiÞcant difference (LSD) method was used to separate treatment means only if the treatment effect was signiÞcant, P ⬍ 0.05. Pair-wise contrast analysis was used compare the combined reßective mulch treatments to the black mulch check. Thrips

species densities and tomato-fruit yield were determined to have a normal distribution, but TSW incidence was arcsine square root transformed before analysis to meet normality assumptions. Means and standard error for the variables were calculated using PROC MEANS procedure of SAS. Not transformed data are presented in the tables and Þgures. Results Reflective Mulch Effect. The average number of F. fusca collected in beat-cup (F ⫽ 5.1; df ⫽ 2, 24; P ⫽ 0.051), blossom (F ⫽ 8.2; df ⫽ 2, 24; P ⫽ 0.019), and sticky trap (F ⫽ 17.1; df ⫽ 2, 6; P ⫽ 0.003) samples over all sample dates were signiÞcantly less on the heatstripe and UV-reßective mulch than on black mulch (Table 1). Likewise, the number of F. fusca captured on sticky traps was signiÞcantly greater on the black mulch treatment than on other mulches at two (F ⫽ 5.2; df ⫽ 2, 6; P ⫽ 0.049), six (F ⫽ 45.9; df ⫽ 2, 6; P ⬍ 0.001), eight (F ⫽ 11.6; df ⫽ 2, 6; P ⫽ 0.009), and 10 (F ⫽ 6.1; df ⫽ 2, 6; P ⫽ 0.036) weeks after transplant (Fig. 1b). Similarly, signiÞcantly greater numbers of F. fusca were observed in blossom samples from the black mulch treatment at six (F ⫽ 13.5; df ⫽ 2, 24; P ⫽ 0.006) and seven (F ⫽ 5.6; df ⫽ 2, 24; P ⫽ 0.042) weeks after transplant (Fig. 1c). The density of F. occidentalis in beat-cup samples did not differ signiÞcantly among mulch treatments overall (Table 1). Average number of total thrips collected in sticky traps was signiÞcantly lower on heat-stripe and UV-reßective mulch treatments than on black mulch treatment (contrast analysis F ⫽ 17.8; df ⫽ 1; P ⫽ 0.006), although mulch types had no signiÞcant effect on average F. occidentalis in beat-cup or blossom overall (Table 1). In 2009, among three harvest dates, fruit yield was greatest during the second harvest when both marketable fruit weight (F ⫽ 6.9; df ⫽ 2, 24; P ⫽ 0.028) and number of fruits (F ⫽ 9.5; df ⫽ 2, 24; P ⫽ 0.014) were signiÞcantly greater on plants raised on heat-stripe or UV-reßective mulch than on black mulch. However, average fruit weight or number harvested over all harvest dates was not signiÞcantly different among mulch treatments (Table 2). TSW incidence was sig-

August 2012


Fig. 1. Effect of mulch treatments on (a) percentage TSW incidence, and thrips (b) F. fusca on yellow sticky traps, (c) F. fusca, and (d) F. occidentalis in beat cup per 10 plants in spring 2009 tomato test at Tifton, GA. The asterisk above a sampling date indicate signiÞcant differences among treatments (*␣ ⫽ 0.05, **␣ ⫽ 0.01, ***␣ ⫽ 0.001).

Table 2. Tifton, GA

niÞcantly greater on black mulch treatments than on other mulch treatments at six (F ⫽ 11.7; df ⫽ 2, 24; P ⫽ 0.009) and 11 (F ⫽ 5.5; df ⫽ 2, 24; P ⫽ 0.042) weeks after transplanting (Fig. 1a). The seasonal accumulation of TSW incidence just before the Þrst harvest was not signiÞcantly different between reßective mulch treatments. However, the reßective mulch treatments produced signiÞcantly lower TSW incidence than the black mulch (Table 2). TSW was deemed the primary cause of tomato yield loss relative to the check. In 2010, the average numbers of F. fusca (F ⫽ 21.6; df ⫽ 2, 6; P ⫽ 0.002) collected on sticky traps, and F. occidentalis (F ⫽ 20.7; df ⫽ 2, 24; P ⫽ 0.002) collected in beat-cup in the heat-stripe or UV-reßective mulch treatments were signiÞcantly smaller than on black mulch treatment (Table 3). In 2010, the average numbers of total thrips (contrast analysis F ⫽ 94.4; df ⫽ 1; P ⬍ 0.001) collected on sticky traps, and total thrips (contrast analysis F ⫽ 35.6; df ⫽ 1; P ⬍ 0.001) collected in beat-cup in the heat-stripe and UV-reßective mulch treatments were signiÞcantly smaller than on black mulch treatment. Likewise, the numbers of F. fusca collected on sticky traps were signiÞcantly greater in the black mulch treatment than the other two mulch treatments for most of the sampling dates including two (F ⫽ 24.2; df ⫽ 2, 6; P ⫽ 0.001), four (F ⫽ 10.9; df ⫽ 2, 6; P ⫽ 0.010), Þve (F ⫽ 44.2; df ⫽ 2, 6; P ⬍ 0.001), six (F ⫽ 21.9; df ⫽ 2, 6; P ⫽ 0.001), seven (F ⫽ 47.6; df ⫽ 2, 6; P ⬍ 0.001), eight (F ⫽ 10.2; df ⫽ 2, 6; P ⫽ 0.011), and nine (F ⫽ 7.9; df ⫽ 2, 6; P ⫽ 0.021) weeks after transplant (Fig. 2b). The average number of F. fusca collected by beat-cup sampling over all sample dates did not vary with mulch type (Table 4). In addition, F. occidentalis numbers were greater on black mulch treatment than on heat-stripe or UV-reßective mulch treatment in beat cup samples for four (F ⫽ 25.9; df ⫽ 2, 24; P ⫽ 0.001) and Þve (F ⫽ 13.1; df ⫽ 2, 24; P ⫽ 0.007) weeks after transplant and blossom samples at six (F ⫽ 21.1; df ⫽ 2, 24; P ⫽ 0.002) weeks after transplanting (Fig. 2d). Unlike in 2009, mulch treatments had no signiÞcant impact on the fruit weight or number in 2010 with the

Effect of mulch types and acibenzolar-S-methyl on the avg fruit yield and TSWV incidence in spring 2009 tomato test at

Treatment Mainplot Black mulch Heat-stripe mulch UV-reßective mulch Subplot Acibenzolar-S-methyl at transplant only Acibenzolar-S-methyl at transplant ⫹ 10d Acibenzolar-S-methyl at transplant ⫹ 10d ⫹ 20d Acibenzolar-S-methyl at transplant ⫹ 10d ⫹ 20d ⫹ 30d Untreated check a

1305

Total marketable fruit

Second-harvest marketable fruit

% TSW incidencea

Wt (kg)

No. fruits

Wt (Kg)

No. fruits

14.3 ⫾ 1.4a 17.7 ⫾ 1.2a 18.7 ⫾ 1.4a

88.5 ⫾ 7.2a 101.6 ⫾ 6.7a 111.4 ⫾ 6.7a

6.7 ⫾ 0.6b 10.7 ⫾ 0.9a 10.5 ⫾ 0.9a

39.7 ⫾ 2.9b 59.7 ⫾ 4.9a 60.3 ⫾ 5.2a

41.8 ⫾ 1.9a 31.2 ⫾ 1.8b 31.2 ⫾ 2.4b

17.3 ⫾ 1.4a 17.1 ⫾ 1.9a 14.6 ⫾ 1.9a 17.9 ⫾ 1.5a 17.6 ⫾ 2.1a

102.4 ⫾ 8.1a 104.9 ⫾ 10.6a 90.7 ⫾ 10.2a 102.0 ⫾ 8.9a 102.5 ⫾ 8.6a

8.9 ⫾ 0.8a 8.6 ⫾ 1.2a 8.5 ⫾ 1.5a 10.7 ⫾ 1.1a 9.6 ⫾ 1.5a

50.7 ⫾ 4.8a 53.6 ⫾ 6.7a 49.8 ⫾ 5.6a 58.7 ⫾ 6.1a 53.5 ⫾ 5.7a

38.9 ⫾ 2.7a 32.5 ⫾ 2.3a 31.9 ⫾ 3.3a 32.5 ⫾ 3.0a 37.8 ⫾ 3.3a

Based on TSWV incidence reported on 4 June 2009. Data were subjected to analysis of variance using generalized linear models. Means in a column within treatment (mainplot or subplot) followed by different letters are signiÞcantly different (P ⬍ 0.05) and were separated using LSD Test.

1306 Table 3.


Vol. 105, no. 4

Effect of mulch types and acibenzolar-S-methyl on thrips numbers in tomato in 2010, Tifton, GA

Treatment

Mainplot Black mulch Heat-stripe mulch UV-reßective mulch Subplot Acibenzolar-S-methyl at transplant only Acibenzolar-S-methyl at transplant ⫹ 10d Acibenzolar-S-methyl at transplant ⫹ 10d ⫹ 20d Acibenzolar-S-methyl at transplant ⫹ 10d ⫹ 20d ⫹ 30d Untreated check

Beat-cup per 10 plants

Blossom sample per 10 plants

F. fusca

F. occidentalis

F. fusca

F. occidentalis

1.6 ⫾ 0.3a 1.5 ⫾ 0.4a 1.2 ⫾ 0.2a

3.9 ⫾ 0.6a 1.4 ⫾ 0.3b 0.9 ⫾ 0.2b

2.4 ⫾ 0.4a 1.6 ⫾ 0.3a 1.9 ⫾ 0.3a

50.8 ⫾ 2.4a 34.9 ⫾ 3.6a 37.7 ⫾ 2.7a

0.4 ⫾ 0.1a 0.4 ⫾ 0.1a 0.3 ⫾ 0.1a 0.4 ⫾ 0.1a 0.3 ⫾ 0.1a

0.5 ⫾ 0.3a 0.5 ⫾ 0.1a 0.5 ⫾ 0.2a 0.7 ⫾ 0.1a 0.4 ⫾ 0.2a

1.6 ⫾ 0.4a 1.8 ⫾ 0.4a 1.9 ⫾ 0.6a 2.2 ⫾ 0.4a 2.2 ⫾ 0.5a

38.1 ⫾ 4.8a 42.1 ⫾ 3.9a 41.3 ⫾ 6.1a 44.9 ⫾ 3.2a 39.2 ⫾ 3.1a

Yellow sticky trap F. fusca

Total thrips

33.1 ⫾ 5.8a 61.1 ⫾ 5.4a 6.3 ⫾ 1.5b 18.2 ⫾ 2.3b 5.6 ⫾ 0.8b 17.6 ⫾ 1.5b Ñ Ñ Ñ Ñ Ñ

Ñ Ñ Ñ Ñ Ñ

Data were subjected to analysis of variance using generalized linear models. Means in a column within treatment (mainplot or subplot) followed by different letters are signiÞcantly different (P ⬍ 0.05) and were separated using LSD Test.

lower incidence of TSW (Table 3). In 2010, even though number of plants with TSW was small compared with disease incidence in 2009, average TSW incidence was signiÞcantly greater (F ⫽ 6.5; df ⫽ 2, 444; P ⫽ 0.032) on plants raised on black mulch than reßective mulches (Table 4). Through the 2010 sea-

Fig. 2. Effect of mulch treatments on (a) percentage TSWV incidence, and thrips (b) F. fusca in yellow sticky traps, (c) F. fusca, and (d) F. occidentalis in beat-cup per 10 subplants in spring 2010 tomato test at Tifton, GA. The asterisk above a sampling date indicate signiÞcant differences among treatments (*␣ ⫽ 0.05, **␣ ⫽ 0.01, ***␣ ⫽ 0.001).

son, black mulch treatment had signiÞcantly a higher percentage incidence of TSW relative to heat-stripe or UV-reßective mulch treatments at eight (F ⫽ 9.8; df ⫽ 2, 24; P ⫽ 0.013) and 10 (F ⫽ 6.5; df ⫽ 2, 24; P ⫽ 0.031) weeks after transplant (Fig. 2a). Acibenzolar-S-Methyl Effect. In 2009, none of the acibenzolar-S-methyl subplot treatments had any signiÞcant effect on thrips numbers (Table 1). However, by 29 May just before harvest, acibenzolar-S-methyl applied at transplant, 10-d, 20-d and at transplant, 10-d, 20-d, and 30-d signiÞcantly reduced TSW incidence when compared with untreated plots (F ⫽ 3.9; df ⫽ 4, 24; P ⫽ 0.013) (Fig. 3a). Thus, multiple applications were needed to provide signiÞcant reduction in TSW. None of the acibenzolar-S-methyl treatments had a signiÞcant effect on marketable fruit yield (Table 2). In 2010, average TSW incidence was signiÞcantly less in plots treated with acibenzolar-S-methyl treatments than in untreated check plots (F ⫽ 5.2; df ⫽ 4, 444; P ⫽ 0.001). No signiÞcant difference was observed in F. fusca or F. occidentalis numbers among subplot treatments (Table 4). For the 14 May 2010 TSW observation, all acibenzolar-S-methyl treatments significantly reduced TSW incidence compared with untreated check regardless of mulch treatments (F ⫽ 3.5; df ⫽ 4, 24; P ⫽ 0.02) (Fig. 3b). In the UV-reßective plots, acibenzolar-S-methyl treatments had signiÞcantly less TSW than the untreated check plots (F ⫽ 4.4; df ⫽ 4, 140; P ⫽ 0.002). On heat-stripe mulch, acibenzolar-S-methyl applied only at transplant, at transplant then at 10-d and 20-d, and at transplant then at 10-d, 20-d, and 30-d reduced TSW incidence compared with untreated plots (F ⫽ 2.9; df ⫽ 4, 140; P ⫽ 0.024). However, no signiÞcant difference was noted among acibenzolar-S-methyl treatments on black mulch. Similar to 2009, acibenzolar-S-methyl treatments had no effect on marketable fruit yield compared with untreated plots in 2010 overall (Table 3). Interactions. In 2009, a signiÞcant interaction between mainplot treatments (plastic mulches) and subplot treatments (acibenzolar-S-methyl) was observed for TSW incidence before Þrst harvest (29 May, F ⫽ 3.2; df ⫽ 8, 24; P ⫽ 0.01; Fig. 4), but not in 2010. In some cases, acibenzolar-S-methyl treatments combined

August 2012 Table 4. Tifton, GA


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Effect of mulch types and acibenzolar-S-methyl on the avg fruit yield and TSWV incidence in spring 2009 tomato test at

Total marketable fruit

Treatment Mainplot Black mulch Heat-stripe mulch UV-reßective mulch Subplot Acibenzolar-S-methyl at transplant only Acibenzolar-S-methyl at transplant ⫹ 10d Acibenzolar-S-methyl at transplant ⫹ 10d ⫹ 20d Acibenzolar-S-methyl at transplant ⫹ 10d ⫹ 20d ⫹ 30d Untreated check

Second-harvest marketable fruit

% TSW incidencea

Wt (kg)

No. fruits

Wt (kg)

No. fruits

9.9 ⫾ 1.0a 10.0 ⫾ 1.3a 10.4 ⫾ 2.8a

56.9 ⫾ 6.2a 60.6 ⫾ 7.1a 65.3 ⫾ 7.2a

6.9 ⫾ 0.9a 7.6 ⫾ 1.1a 7.5 ⫾ 1.2a

41.1 ⫾ 5.4a 46.1 ⫾ 6.6a 47.2 ⫾ 7.7a

3.3 ⫾ 0.7a 0.8 ⫾ 0.5b 0.7 ⫾ 0.3b

9.2 ⫾ 1.5a 10.7 ⫾ 1.9a 10.2 ⫾ 1.5a 10.1 ⫾ 1.4a 10.2 ⫾ 1.3a

56.7 ⫾ 10.3a 65.5 ⫾ 10.7a 61.4 ⫾ 8.5a 54.4 ⫾ 7.8a 64.4 ⫾ 8.6a

6.1 ⫾ 1.4a 8.8 ⫾ 1.7a 7.3 ⫾ 1.2a 6.9 ⫾ 1.3a 7.3 ⫾ 1.2a

43.4 ⫾ 10.1a 53.3 ⫾ 9.7a 43.4 ⫾ 6.9a 37.0 ⫾ 7.2a 47.5 ⫾ 8.7a

1.1 ⫾ 0.9a 1.4 ⫾ 0.6a 1.1 ⫾ 0.5a 2.2 ⫾ 0.9a 2.2 ⫾ 0.7a

a

Based on TSWV incidence reported on 20 May 2010. Data were subjected to analysis of variance using generalized linear models. Means in a column within treatment (mainplot or subplot) followed by different letters are signiÞcantly different (P ⬍ 0.05) and were separated using LSD Test.

with UV-reßective mulch resulted in a signiÞcant reduction in TSW prevalence and number of vectors captured (Fig. 4; Table 1). In addition, under the low TSW incidence in 2010 all acibenzolar-S-methyl treatments worked equally well, but under the higher incidence in 2009, greater frequency of acibenzolar-Smethyl applications were required to signiÞcantly reduce TSW (Fig. 3). In 2009 and 2010, no signiÞcant mulch ⫻ acibenzolar-S-methyl treatment interaction was observed for F. fusca, F. occidentalis, or on any date or overall (overall 2009, F ⫽ 1.2; df ⫽ 8, 24; P ⫽ 0.36 [F. fusca], F ⫽ 1.9; df ⫽ 8, 24; P ⫽ 0.1 [F. occidentalis], F ⫽ 1.7; df ⫽ 8, 24; P ⫽ 0.16 [total thrips], overall 2010, F ⫽ 1.1; df ⫽ 8, 24; P ⫽ 0.39 [F. fusca], F ⫽ 0.4; df ⫽ 8, 24; P ⫽ 0.92 [F. occidentalis], F ⫽ 0.6; df ⫽ 8, 24; P ⫽ 0.810 [total thrips], respectively). Neither were there

signiÞcant interaction effects on weight of marketable fruit yield in 2009 and 2010 (F ⫽ 1.2; df ⫽ 8, 24; P ⫽ 0.370 and F ⫽ 1.9; df ⫽ 8, 24; P ⫽ 0.090, respectively). Thus, the only signiÞcant interaction observed between acibenzolar-S-methyl treatments and mulch type was relative to the incidence of TSW. Tomato yield in untreated black mulch treatments in 2009 and 2010 (kilogram per subplot ⫾ SD: 16.4 ⫾ 5.5 and 7.4 ⫾ 3.1, respectively) was numerically less than that of the best mulch combination, heat stripe reßective mulch plus 1Ð2 applications of acibenzolar-S-methyl, for each year (kilogram per subplot ⫾ SE: 20.9 ⫾ 4.0 and 14.8 ⫾ 8.8, respectively) by 22 and 50%, respectively. Thus, there was a trend toward beneÞcial yield effects from the combination treatments. Discussion These results are consistent with those of Momol et al. (2004) in that metalized reßective mulch reduces both the incidence of TSW and thrips. In addition, the use of acibenzolar-S-methyl at transplant plus addi-

Fig. 3. Mean (⫾SE) percent TSWV incidence on subplot treatments on 29 May 2009, (a), and 14 May 2010, (b). The abbreviations are: T1 ⫽ acibenzolar-S-methyl at transplant only, T2 ⫽ acibenzolar-S-methyl at transplant ⫹ 10-d, T3 ⫽ acibenzolar-S-methyl at transplant ⫹ 10-d ⫹ 20-d, T4 ⫽ acibenzolar-S-methyl at transplant ⫹ 10-d ⫹ 20-d ⫹ 30-d, and T5 ⫽ Untreated check. Bars with the same letters are not signiÞcantly different (␣ ⫽ 0.05).

Fig. 4. Mean (⫾SE) of percentage TSWV incidence on mainplots and subplot treatments in 2009. Bars with similar case letters are not signiÞcantly different within mulch types (␣ ⫽ 0.05).

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tional foliar treatments reduced the incidence of TSW. The use of acibenzolar-S-methyl may function better in reducing TSW in conjunction with solid metalized UV-reßective mulch than on black plastic based on the interaction found in this study. Under higher TSW incidence in the Þeld in 2009, at least a transplant application plus two foliar sprays spaced 10 d apart of acibenzolar-S-methyl were required to receive a signiÞcant beneÞt from this treatment. At the lower incidence of TSW in 2010, the reduction of TSW relative to the check was signiÞcant for all of the acibenzolarS-methyl treatments. There was no signiÞcant difference between UVreßective and heat-stripe mulch (25% less reßective surface) on thrips or TSW incidence. Heat-stripe mulch has a middle black stripe with UV-reßective surface on either side. Previously, it has been shown that the UV-reßective mulch could cool soil temperatures by as much as 2⬚C, which can retard plant growth and delay crop maturity (Diaz and Batal 2002). Using a “heat-stripe” mulch to lessen the intensity of this soil cooling effect could have merit based on our results demonstrating that reductions in thrips numbers and TSW incidence were not signiÞcantly sacriÞced compared with the complete UV-reßective mulch. However, both reßective mulch types yielded more than the black plastic mulch treatment and there was no signiÞcant delayed yield. Thus, the cost of the reßective plastic mulches would be the only critical factor in determining its use. In general, the use of reßective mulches could be a way to reduce heavy dependence on insecticide aimed at suppressing thrips vectorsÕ populations, which often leads to the development of insecticide resistance (Bielza 2008). Where disposal of plastic mulches is a concern, other reßective, environmentally friendly soil Þlm options are a possibility (Glenn and Puterka 2004, Reitz et al. 2008). Healthy tomato plants have a natural physiological ability to resist invading pathogens. This natural defense reaction can be enhanced by acibenzolar-Smethyl applications (Pappu et al. 2000, Mandal et al. 2008). Acibenzolar-S-methyl apparently has no effect on F. fusca and F. occidentalis; its primary effect is believed to be activation of the salicylic acid pathway, whereas, the jasmonic acid pathway is primarily responsible for resistance against herbivores (Eyles et al. 2009). In our study, the effect of acibenzolar-S-methyl applied at various times provided some reduction of TSW incidence without affecting thrips numbers, but the effect was not sufÞcient to prevent yield loss. In 2010, under low disease pressure, even the acibenzolar-S-methyl applied only at transplant resulted in signiÞcant suppression of TSW incidence on tomato plants. In particular, the acibenzolar-S-methyl treated subplots on UV-reßective mulches had fewer TSW symptomatic plants than in untreated plots. However, these differences in TSW incidence in acibenzolar-Smethyl treatments did not signiÞcantly increase marketable fruit yield. Momol et al. (2004) also reported a similar reduction in TSW incidence without a consistent increase in marketable fruit yield after season-

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long applications of acibenzolar-S-methyl. Acibenzolar-S-methyl in conjunction with imidacloprid has been shown to be very effective in reducing early season TSW incidence in tobacco (McPherson et al. 2005, Pappu et al. 2000). This plus our results suggest that use of acibenzolar-S-methyl might require the use of an additional thrips reducing tactic to provide signiÞcant reductions in disease incidence. What is interesting from our results is that signiÞcant TSW reduction could occur with very few or only one transplant application of acibenzolar-S-methyl when disease pressure was low. Recently, growers have embraced TSW-resistant cultivars based on a single SW5 gene to overcome the TSW problem (Krishna Kumar et al. 1993, 1995; Saidi and Warade 2008; Riley et al. 2011). Even so, extensive dependence on a single gene for resistance might generate high selection pressure on the local TSWV isolates, which can result in resistance failure (Thomas-Carroll and Jones 2003, Aramburu and Marti 2003, Ciuffo et al. 2005). Therefore, it is important to continue developing an integrated thrips vector management options for possible loss of resistance and/or the cultivation of popular TSW susceptible cultivars. The most common management options other than host plant resistance include reßective mulches, insecticides, and timely applications of plant defense activators (Cho et al. 1989; Greenough et al. 1990; Kring and Schuster 1992; Bauske et al. 1998; Olson et al. 2000; Riley and Pappu 2000; Reitz et al. 2003; Diaz et al. 2003, 2007; Momol et al. 2004; Riley and Pappu 2004; Jacobson and Kennedy 2011). Our study conÞrmed that reßective mulches can signiÞcantly reduce thrips population density and TSW incidence in the tomato crop. In our study, marketable yield increased up to 22Ð50% in some combination treatments. Although use of UVreßective mulch and acibenzolar-S-methyl could increase production cost by up to $373/ha, it has been shown to be cost effective (Fonsah et al. 2010).

Acknowledgment We acknowledge the Vegetable Entomology Laboratory personnel J. Davis, D. Cook, J. Kicklighter, and J. Sumner for their help during these trials. This study was supported by the Georgia Agricultural Experiment Stations and USDA RAMP grant project number GEO-2008-02924.

References Cited Aramburu, J., and Martı´ M. 2003. The occurrence in northeast Spain of a variant of Tomato spotted wilt virus (TSWV) that breaks resistance in tomato (Lycopersicon esculentum) containing the Sw-5 gene. Plant Pathol. 52: 407Ð 407. Bauske, E. M., G. M. Zehnder, E. J. Sikora, and J. Kemble. 1998. Southeastern tomato growers adopt integrated pest management. HortTechnol. 8: 40 Ð 44. Best, R. J. 1968. Tomato spotted wilt virus, pp. 65Ð146. In K. M. Smith and M. A. Lauffer (eds.), Advances in virus research, vol. 13. Academic, New York.

August 2012


Bielza, P. 2008. Insecticide resistance management strategies against the western ßower thrips, Frankliniella occidentalis. Pest Manage. Sci. 64: 1131Ð1138. Cho, J. J., R.F.L. Mau, T. L. German, R. W. Hartmann, L. S. Yudin, D. Gonsalves, and R. Provvidenti. 1989. A multidisciplinary approach to management of tomato spotted wilt virus in Hawaii. Plant Dis. 62: 264 Ð272. Cho, K. J., C. S. Eckel, J. F. Walgenbach, and G. G. Kennedy. 1995. Comparison of colored sticky traps for monitoring thrips populations (thysanoptera, Thripidae) in staked tomato Þelds. J. Entomol. Sci. 30: 176 Ð190. Ciuffo, M., M. M. Finetti-Sialer, D. Gallitelli, and M. Turina. 2005. First report in Italy of a resistance-breaking strain of Tomato spotted wilt virus infecting tomato cultivars carrying the Sw5 resistance gene. Plant Pathol. 54: 564. Dıáz-Pe´rez, J. C., and K. D. Batal. 2002. Colored plastic Þlm mulches affect tomato growth and yield via changes in root-zone temperature. J. Am. Soc. Hortic. Sci. 127: 127Ð 136. Dıáz-Pe´rez, J. C., K. D. Batal, D. Granberry, D. Bertrand, D. Giddings, and H. Pappu. 2003. Growth and yield of tomato on plastic Þlm mulches as affected by Tomato Spotted Wilt Virus. HortScience 38: 395Ð399. Dıáz-Pe´rez, J. C., R. Gitaitis, and B. Mandal. 2007. Effects of plastic mulches on root zone temperature and on the manifestation of tomato spotted wilt symptoms and yield of tomato. Sci. Hort. 114: 290 Ð95. Eyles, A., P. Bonello, R. Ganley, and C. Mohammed. 2009. Induced resistance to pests and pathogens in trees. New Phytol. 185: 893Ð908. Fonsah, E. G., C. M. Ferrer, D. G. Riley, S. Sparks, and David Langston. 2010. Cost and beneÞt analysis of Tomato spotted wilt virus (TSWV) management technology in Georgia. The Southern Agricultural Economic Association Conference (SAEA). (http://ageconsearch.umn. edu/bitstream/56386/2/51028.pdf). Gitaitis, R. 2009. Tospoviruses in Georgia vegetables. In Tospoviruses in Solanaceae and other crops in the coastal plain of Georgia, pp. 24 Ð27. College of Agricultural and Environmental Sciences, Athens, GA. Bull. 1354. Glenn, D. M., and G. J. Puterka. 2004. Particle Þlm technology: a new tool for agriculture. Horticultural Rev. 31: 1Ð 45. Goldbach, R., and D. Peters. 1994. Possible causes of the emergence of tospovirus diseases. Semin. Virol. 5: 113Ð 120. Gordillo, L. F., M. R. Stevens, M. A. Millard, and B. Geary. 2008. Screening two Lycopersicon peruvianum collections for resistance to Tomato spotted wilt virus. Plant Dis. 92: 694 Ð704. Greenough, D. R., L. L. Black, and W. P. Bond. 1990. Aluminum-surfaced mulch: an approach to the control of tomato spotted wilt virus in solanaceous crops. Plant Dis. 74: 805Ð 808. Jacobson, A. L., and G. G. Kennedy. 2011. The effect of three rates of cyantraniliprole on the transmission of tomato spotted wilt virus by Frankliniella occidentalis and Frankliniella fusca (Thysanoptera: Thripidae) to Capsicum annuum. Crop Prot. 30: 512Ð515. Jones, D. R. 2005. Plant viruses transmitted by thrips. Euro. J. Plant Pathol. 113: 119 Ð157. Joost, P. H., and D. G. Riley. 2004. Sampling techniques for thrips (Thysanoptera: Thripidae) in pre-ßowering tomato. J. Econ. Entomol. 97: 1450 Ð1454. Joost, P. H., and D. G. Riley. 2005. Imidacloprid effects on probing and settling behavior of Frankliniella fusca and Frankliniella occidentalis (Thysanoptera: Thripidae) in tomato. J. Econ. Entomol. 98: 1622Ð1629.

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Kring, J. B., and D. J. Schuster. 1992. Management of insects on pepper and tomato with UV-reßective mulches. Fla. Entomol. 75: 119 Ð129. Krishna Kumar, N. K., D. E. Ullman, and J. J. Cho. 1993. Evaluation of Lycopersicon germplasm for tomato spotted wilt tospovirus resistance by mechanical and thrips transmission. Plant Dis. 77: 938 Ð941. Krishna Kumar, N. K., D. E. Ullman, and J. J. Cho. 1995. Resistance among Lycopersicon species to Frankliniella occidentalis (Thysanoptera: Thripidae). J. Econ. Entomol. 88: 1057Ð1065. Latham, L. J., and R.A.C. Jones. 1998. Selection of resistance breaking strains of Tomato spotted wilt tospovirus. Ann. Appl. Biol. 133: 385Ð 402. Mandal, B., S. Mandal, A. S. Csinos, N. Martinez, A. K. Culbreath, and H. R. Pappu. 2008. Biological and molecular analyses of the acibenzolar-S-methyl-induced systemic acquired resistance in ßue-cured tobacco against tomato spotted wilt virus. Phytopathology 98: 196 Ð204. McPherson, R. M., M. G. Stephenson, S. S. LaHue, and S. W. Mullis. 2005. Impact of early-season thrips management on reducing the risks of spotted wilt virus and suppressing aphid populations in ßue-cured tobacco. J. Econ. Entomol. 98: 129 Ð134. Momol, M. T., S. M. Olson, J. E. Funderburk, J. Stavisky, and J. J. Marois. 2004. Integrated management of tomato spotted wilt on Þeld-grown tomatoes. Plant Dis. 88: 882Ð 890. Oetting, R. D., R. J. Beshear, T.-X. Liu, S. K. Braman, and J. R. Baker. 1993. Biology and identiÞcation of thrips on greenhouse ornamentals. Georgia Agricultural Experiment Station. Res. Bull. 414. Olson, S. M. 2009. Physiological, nutritional, and other disorders of tomato fruit. University of Florida Publ. HS-954. (http://edis.ifas.uß.edu/hs200). Olson, S., J. Stavesky, T. Momol, and J. Funderburk. 2000. Reßective mulches and their effect on tomato yield and insect and disease management. Proc. Natl. Agric. Plastics Cong. 29: 605Ð 609. Pappu, H. R., A. S. Csinos, R. M. McPherson, D. C. Jones, and M. G. Stephenson. 2000. Effect of acibenzolar-S-methyl and imidacloprid on suppression of tomato spotted wilt Tospovirus in ßue-cured tobacco. Crop Prot. 19: 349 Ð354. Persley, D. M., J. E. Thomas, and M. Sharman. 2006. Tospoviruses: an Australian perspective. Australas Plant Path. 35: 161Ð180. Reitz, S. R., E. L. Yearby, J. E. Funderburk, J. Stavisky, M. T. Momol, and S. M. Olson. 2003. Integrated management tactics for Frankliniella thrips (Thysanoptera: Thripidae) in Þeld-grown peppers. J. Econ. Entomol. 96: 1201Ð1214. Reitz, S. R., G. Maiorino, S. Olson, R. Sprenkel, A. Crescenzi, and M. T. Momol. 2008. Integrating plant essential oils and kaolin for the sustainable management of thrips and tomato spotted wilt on tomato. Plant Dis. 92: 878 Ð 886. Riley, D. G., and H. R. Pappu. 2000. Evaluation of tactics for management of thrips-vectored tomato spotted wilt Tospovirus in tomato. Plant Dis. 84: 847Ð 852. Riley, D. G., and H. R. Pappu. 2004. Tactics for management of thrips (Thysanoptera: Thripidae) and Tomato Spotted Wilt Virus in tomato. J. Econ. Entomol. 97: 1648 Ð 1658. Riley, D. G., S. V. Joseph, R. Srinivasan, and S. Diffie. 2011a. Thrips vectors of Tospoviruses. J. Integrated Pest Manage. 1: 2011. (doi:10.1603/IPM10020). Riley, D. G., S. V. Joseph, W. T. Kelley, S. Olson, and J. Scott. 2011b. Host plant resistance to Tomato spotted wilt virus (Bunyaviridae: Tospovirus) in tomato. HortScience 46: 1626 Ð1633.

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Saidi, M., and S. D. Warade. 2008. Tomato breeding for resistance to Tomato spotted wilt virus (TSWV): an overview of conventional and molecular approaches. Czech. J. Genet. Plant Breed 44: 83Ð92. Sargent, S. A., and C. L. Moretti. 2004. The commercial storage of fruits, vegetables, and ßorist and nursery stocks: tomato. USDA, ARS Agriculture Handbook 66. (http:// www.ba.ars.usda.gov/hb66/138tomato.pdf). SAS Institute. 2008. UserÕs manual, version 9.1 SAS Institute, Cary, NC. Stannard, L. J. 1968. The thrips, or Thysanoptera of Illinois. Ill. Nat. Hist. Surv. Bull. 29: 215Ð552. Stevens, M. R., S. J. Scott, and R. C. Gergerich. 1992. Inheritance of a gene for resistance to tomato spotted wilt virus (TSWV) from Lycopersicon peruvianum Mill. Euphytica 59: 9 Ð17.

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Stevens, M. R., J. W. Scott, B. D. Geary, J. J. Cho, L. F. Gordillo, D. M. Persley, F. D. Memmott, and J. J. Stevens. 2006. Current status of resistance to Tospoviruses in tomato. Tampa, 7Ð11 May 2006, Tomato Breeders Roundtable and Tomato Quality Workshop abstr. 34. Thomas-Carroll, M. L., and R.A.C. Jones. 2003. Selection, biological properties and Þtness of resistance-breaking strains of Tomato spotted wilt virus in pepper. Ann. Appl. Biol. 142: 235Ð243. Ullman, D. E., J. L. Sherwood, and T. L. German. 1997. Thrips as vectors of plant pathogens, pp. 539 Ð565. In T. Lewis (ed.), Thrips as crop pests. CAB International, Wallingford, Oxon, United Kingdom. Received 27 May 2011; accepted 17 April 2012.