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Crop Protection 30 (2011) 1178e1183

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Crop Protection

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Chemical control of the European tarnished plant bug, Lygus rugulipennis,on strawberry in the UK

Jean Fitzgerald*, Chantelle JayEast Malling Research, New Road, East Malling, Kent ME19 6BJ, UK

a r t i c l e i n f o

Article history:Received 5 November 2010Received in revised form15 April 2011Accepted 18 April 2011

Keywords:Lygus rugulipennisDevelopmental stagesBifenthrinThiaclopridAcetamipridFlonicamidLambda cyhalothrinIndoxacarbEtoxazoleSurfactant

* Corresponding author. Tel.: þ44 (0) 1732 523758E-mail address: jean.fitzgerald@emr.ac.uk (J. Fitzg

0261-2194/$ e see front matter � 2011 Elsevier Ltd.doi:10.1016/j.cropro.2011.04.006

a b s t r a c t

European tarnished plant bug, Lygus rugulipennis, is a serious pest on late season strawberries in the UK.Feeding by the pest on the developing fruits causes severe malformation, and over 50% of fruit may bedowngraded as a result of capsid feeding in unsprayed crops. A range of compounds was tested againstthe pest over two years at East Malling Research. In 2008 experiments were conducted on weed plotswith high L. rugulipennis populations, and in 2009 were conducted on an everbearer strawberry planting.The 2008 experiments showed that etoxazole had no effect on L. rugulipennis and that although floni-camid and indoxacarb significantly reduced populations they were not as effective as thiacloprid, eitherwith or without a surfactant, or acetamiprid. In the 2009 experiment on strawberry thiaclo-prid þ surfactant, applied twice, was more effective than this treatment applied once, which in turn wasmore effective than thiacloprid alone. In both years the most effective treatment was the pyrethroidbifenthrin. There was no suggestion that different developmental stages of the pest were moresusceptible to the tested insecticides. Thus there was no evidence to suggest that timing applicationsagainst specific life stages would significantly improve pest control.

� 2011 Elsevier Ltd. All rights reserved.

1. Introduction

The European tarnished plant bug, Lygus rugulipennis Poppius, isa serious pest on late season strawberries in the UK (Easterbrook,2000). Feeding by the pest on the developing fruits causes severemalformation and over 50% of fruit may be downgraded as a resultof capsid feeding in unsprayed crops (Jay et al., 2004). In the relatedspecies Lygus lineolaris (Palisot de Beauvois) Rhainds and English-Loeb (2003) showed that the variety of strawberry did not affectoviposition preferences of the females. However, resistance wasdetected to this pest in some named varieties and advancedselections of Fragaria � ananassa L. by Dale et al. (2008). Also infield experiments in the UK the variety Bolerowas found to bemoresusceptible to feeding damage by L. rugulipennis than other varie-ties tested (Easterbrook and Simpson, 2000). In PolandL. rugulipennis feeding damage was also shown to be related tostrawberry variety, with damage of up to 40% seen on some vari-eties (Labanowska, 2007). Damage has been shown to be depen-dant on the age of the flower or fruit when feeding occurred(Easterbrook, 1996).

; fax: þ44 (0) 1732 849067.erald).

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L. rugulipennis overwinters in the adult stage. In the UK the firstgeneration develops mainly on various weed species in spring andearly summer, with adults developing in June and July(Easterbrook, 1997). These adults migrate to flowering strawberrieswhen themajority of weeds senesce and eggs are laid in strawberrybetween July and September. There are two or three generationsper year. In Italy there are reported to be 3e4 generations per year(Rancati et al., 1996); development from egg to egg took 36 days inJuly. In laboratory experiments (Easterbrook et al., 2003) the meandevelopment time from egg lay to adulthood ranged from 66 daysat a constant 15 �C to 22 days at 25 �C when L. rugulipennis wasreared on groundsel (Senecio vulgaris), one of the weed speciesfavoured by the pest. No eggs hatched below 10 �C. Developmenttimes were slightly longer on strawberry at the same temperatures.The temperature at which overwintered adults become active wasnot recorded in these experiments. Thus the actual timing ofcolonisation of strawberry by L. rugulipennis cannot currently bepredicted from temperature data alone, and careful monitoring ofthe crop and surrounding weeds is required by growers to deter-mine if insecticide applications are required against the pest.

The mean fecundity of L. rugulipennis at 20 �C was 75 eggsper female (Easterbrook et al., 2003). Thus there is the potential fora rapid increase in numbers of L. rugulipennis in the crop afterthe immigration of the adults from weeds. Nymphs and adults

J. Fitzgerald, C. Jay / Crop Protection 30 (2011) 1178e1183 1179

developing from the eggs laid on the strawberry plant feed on thedeveloping fruits and cause severe damage. The period from lateJuly to late August is when most feeding damage in flowers isinitiated; there is a 3e4 week interval between the initiation ofdamage and picking of the damaged fruit. As these insects are verymobile, significant fruit damage can be caused by low populationsof the pest. However, previous research (Easterbrook, 2000; Jayet al., 2004) has shown a significant correlation between fruitdamage and numbers of capsids present in the crop.

Currently, no biocontrol agents are commercially available forL. rugulipennis, although research in Canada and the USA has sug-gested that the braconid parasitoids Peristenus relictus Loan andPeristenus digoneutis Loan can reduce Lygus populations in crops(Haye et al., 2005; Pickett et al., 2009). Therefore growers are relianton insecticides to prevent damage to the crop. Pyrethroids, such asbifenthrin, are effective against L. rugulipennis. However, theyshould not be applied when the plants are flowering as they aretoxic to bees. Therefore they are difficult to use on everbearingstrawberries which have a long flowering period. Pyrethroids arealso damaging to biocontrol agents used against other pests instrawberry, such as the predatory mite Phytoseiulus persimilisAthias-Henriot, which is used against the glasshouse spider miteTetranychus urticae Koch, and Neoseiulus (Amblyseius) cucumeris(Oudemans), which is used against tarsonemid mites Phytonemuspallidus (Banks) andWestern flower thrips Frankliniella occidentalis(Pergande). Thus they are not compatible with IPM techniques.Approval for use of bifenthrin against L. rugulipennis on strawberrywill be revoked in 2011. In the UK there is a specific off labelapproval (SOLA) for the use of thiacloprid against L. rugulipennis,but its use has not always given significant reductions in fruitdamage. Therefore there is a lack of practical options for chemicalcontrol of this pest. Fitzgerald (2004) showed that thiacloprid wasmore effective against L. rugulipennis nymphs than adults. Thus thereported inconsistent results with thiacloprid may be due toincorrect timing of application with respect to the developmentalstages of the pest present, and it is possible that other insecticidesalso have different effects on nymphs and adults. Since control ofthis pest in the UK has relied on two active ingredients, alternativechemical control techniques, ormore effective timing of applicationof currently available products, are needed for this pest. Ideallyinsecticides used to control L. rugulipennis should be compatiblewith overall IPM programmes for other strawberry pests and besafe to apply during flowering of the crop, i.e. be non-toxic topollinators.

Against a background of reduced availability of chemical controloptions for L. rugulipennis, the aims of this research were to assessthe efficacy of a range of chemical treatments and to determine if

Table 1Treatments applied against L. rugulipennis in 2008 (year 1) and 2009 (year 2). Sprays werein year 2.

Active ingredient and formulation Product

Bifenthrin 80 g/l SC BrigadeThiacloprid 480 g/l SC CalypsoThiacloprid þ surfactant Calypso þ Break Thru S240Thiacloprid þ surfactant

� 2 applicationsCalypso þ Break Thru S240� 2 applications

Acetamiprid 20% w/w SP GazelleFlonicamid 50% w/w WG MainmanLambda cyhalothrin 100 g/l CS HallmarkIndoxacarb 30% w/w WG StewardEtoxazole 110 g/l SC Borneoe Untreated

Only bifenthrin had full approval for use on strawberry at the time the experiments werecurrently has approval for use on strawberry in the UK.

applications timed to target specific life stages of the pest weremore effective. As large populations of L. rugulipennis develop onflowering weed species before dispersing to other plants, includingflowering strawberry, three replicated experiments were con-ducted in 2008 on weed plots. Chemicals to be tested were chosenon the basis of unpublished reports of their efficacy on relatedspecies and on their suitability for use within IPM systems;a pyrethroid was used as a standard control chemical. Since timingof application, with respect to the life stages of L. rugulipennispresent, may be critical for the effectiveness of the treatments,capsid population development within flowering weed plots wasmonitored and the proportion of each life stage present recorded.Chemical treatments were then applied to target peaks of thedifferent life stages of the pest to determine if some stages weremore susceptible than others. Results from 2008 were used todetermine the most effective compounds to be used in a replicatedexperiment in 2009 on everbearing strawberries.

2. Materials and methods

2.1. 2008 Experiments

In 2008, self-seeded weed plots at East Malling Research (EMR)were used in the three experiments that were conducted. The mainspecies present in these weed plots was mayweed (Matricaria sp.),and a different patch of weeds was used for each experiment. Eachexperiment was a randomised complete block design. Plots were2.5 m wide and 4 m long. Experiment 1 was timed to target a peakof 1st and 2nd instar L. rugulipennis nymphs, experiment 2 targeted3rde5th instar nymphs and experiment 3 targeted adults. Dates ofapplication of pesticides were based on relative numbers of thedifferent life stages recorded in tap samples of the plants. Therewere five blocks in experiment 1 and four blocks in experiments 2and 3, with each block containing a single plot of each treatment.The same nine treatments were evaluated in each experiment.Treatments were single sprays applied with a motorised knapsacksprayer with a hand-lance at a volume rate of 1000 l/ha (Table 1).Applications in experiments 1, 2 and 3 were made on 7 and 20August and on 11 September respectively.

Tap sampling was used for pre-treatment and the first post-treatment sample when assessing effects on L. rugulipennisnymphs. L. rugulipennis nymphs were identified in the field andwere returned to the plants to reduce the impact of sampling on thepest population. Sweep sampling was used for the final samplingoccasion when impact on the remaining population was notimportant. Arthropods captured in the sweep samples were iden-tified in the laboratory. When assessing the impact of insecticides

applied at a volume rate of 1000 l/ha toweed plots in year 1 and to strawberry plants

Dose rate a.i. per ha Year tested

24 g 1, 2120 g 1, 2

120 g þ 300 ml 1, 2120 g þ 300 ml 2

75 g 1, 270 g 17.5 g 175 g 1

49.5 g 1e 1, 2

conducted and there is a SOLA for the use of thiacloprid; none of the other products

J. Fitzgerald, C. Jay / Crop Protection 30 (2011) 1178e11831180

on mobile adult L. rugulipennis, sweep sampling was used for bothpost-treatment assessments. Numbers of individuals captured bythe two sampling techniques may differ so numbers caught by thetwo sampling techniques cannot be directly compared.

For experiment 1 a pre-treatment samplewas taken on 6 August2008. Plants were tapped over a 13 cm diameter white dish andnumbers of each of the L. rugulipennis life stages present recorded.The first post-treatment sample was taken on 11 August (4 daysafter treatment e DAT); this was also a tap sample with 10 tapstaken per plot over a white bowl. Individuals from both sampleswere returned to the plants. The second post-treatment samplewas taken on 19 August (12 DAT); this sample was 10 sweeps perplot using a 45 cm diameter sweep net. All developmental stageswere recorded in all samples.

The relative proportions of the different life cycle stages recor-ded in the untreated plots on 19 August in experiment 1 indicatedthat the treatment to target late instar nymphs in experiment 2should be applied immediately. A tap sample was taken on 21August (1 DAT) and a sweep sample on 28 August (8 DAT). Alldevelopmental stages were recorded in both samples.

For experiment 3, targeting adults, sweep samples were takenon 13 September (1 DAT) and on 17 September (5 DAT). All devel-opmental stages were recorded in both samples.

2.2. 2009 Experiment

In 2009 the most effective treatments from the 2008 experi-ments were tested on strawberry. A one-year old strawberryplanting of cultivar Evie 2 was used for this experiment at EastMalling Research. The experiment was a randomised completeblock design with five blocks. Each plot was one strawberry bed,0.8 m wide and 8.6 m long. Beds were 3 m apart to prevent anycontamination from spray drift. Plots were 3 m apart in the bed.Treatments were single sprays applied with a motorised knapsacksprayer with a hand-lance at a volume rate of 1000 l/ha exceptthere was a repeat application of thiacloprid þ surfactant (Table 1).The pesticides were applied on 28 July with the 2nd application ofthiacloprid plus surfactant being applied on 11 August.

L. rugulipennis were assessed on all plots as described for the2008 experiments. Assessments were made before the first treat-ment, 3 and 9 days after the first pesticide application, and 3 and 9days after the second application of thiacloprid plus surfactant. Thedifferent developmental stages of L. rugulipennis present wererecorded.

2.3. Statistical analysis

For each of the three experiments in 2008, there were twosampling dates post-treatment. Numbers recorded on these twodates were analysed as a split-plot design, with time being thesplit-plot factor and treatment the main plot factor. Residual plotsafter analyses of the raw count data indicated increasing variancewith increasing mean; much greater variance homogeneity wasobtained by using a square root transformation of the counts priorto analysis throughout. Following the ANOVAs, treatment and timeeffects were assessed from the resultant variance ratio tests usingthe F-probability values, and appropriate t-tests made to comparemeans on the transformed scale. For the 2009 experiment, therewere two assessments before and two assessments after the secondapplication of thiacloprid þ surfactant and these two sets of datawere analysed separately to account for differing sets of treatmentsapplied for the two periods, again as a split-plot design. Counts ofeach developmental stage were square root transformed as beforeto improve variance homogeneity and appropriate t-tests used tocompare means on the transformed scale after the variance ratio

tests. Where pre-treatment counts were made, these were initiallyused as covariates (on the square root scale to match the analyseddata), but in no case was the covariate significant so the resultspresented are without use of covariates. All analyses were carriedout using GenStat 9th edition (Payne et al., 2006).

3. Results

3.1. 2008 Experiments

Although the 2008 experiments specifically targeted particularlife stages of L. rugulipennis, numbers of insects in other develop-mental stages were recorded during sampling and these were thenanalysed separately for each experiment to obtain additionalinformation on the effects of the test compounds on these lifestages.

In the pre-treatment sample for experiment 1, the proportionsof the different life stages of L. rugulipennis present were 68%instars 1e2; 20% instars 3e5; 12% adults. There were significantdifferences between treatments on both sample dates (F ¼ 57.94;df ¼ 8, 32; p < 0.001) for young nymphs, (F ¼ 46.09; df ¼ 8, 32;p < 0.001) for older nymphs (F ¼ 2.25; df ¼ 8, 32; p ¼ 0.05) foradults. For the targeted stage, young nymphs, there was no indi-cation of any overall time differences (F ¼ 0.08; df ¼ 1, 36;p ¼ 0.782) nor of an interaction between treatment and time(F ¼ 0.53; df ¼ 8, 36; p ¼ 0.826) so the overall treatment means areshown in Table 2. For adults there was no significant interactionbetween treatment and time (F ¼ 0.84; df ¼ 8, 36; p ¼ 0.575),although there was an overall difference between times (F ¼ 21.50;df ¼ 1, 36; p < 0.001) with counts higher for the later time. For theolder nymphs there was a time by treatment interaction (F ¼ 5.54;df ¼ 8, 36; p < 0.001) with the effect of thiacloprid þ surfactantgreater at 12 than 4 DAT, possibly indicating a slower mode ofaction of this product.

At the time of application of treatments in the second experi-ment targeting 3rd, 4th and 5th instar nymphs the proportions ofthe different life stages of L. rugulipennis present were 50% instars1e2; 44% instars 3e5; 6% adults. There were significant differencesbetween treatments on both sample dates (F ¼ 23.48; df ¼ 8, 24;p < 0.001) for young nymphs (F ¼ 33.74; df ¼ 8, 24; p < 0.001) forolder nymphs and (F ¼ 6.26; df ¼ 8, 24 p < 0.001) for adults. As inexperiment 1, there was no significant time by treatment interac-tion for the target group (instars 3e5) (F ¼ 1.66; df ¼ 8, 27;p ¼ 0.154) so the overall treatment means are shown in Table 2.There was some evidence of overall differences between the twotimes (F ¼ 6.62; df ¼ 1, 27; p ¼ 0.016) with counts higher for thelater time. For the 1st and 2nd instars there was an interaction(F ¼ 4.48; df ¼ 8, 27; p ¼ 0.002) with numbers increasing in alltreatments except the bifenthrin and lambda cyhalothrin treat-ments between 1 and 8 DAT, indicating a persistent effect of thepyrethroids on eggs and/or newly hatched nymphs. There was notime by treatment interaction for adults (F ¼ 0.74; df ¼ 8, 27;p ¼ 0.652) although the overall time effect was highly significant(F¼ 14.64; df¼ 1, 27; p< 0.001) with the later time higher than theearlier.

At the beginning of the third experiment targeting adults theproportions of the different life stages of L. rugulipennis presentwere 9% instars 1e2; 42% instars 3e5; 49% adults. There weresignificant differences between treatments on both sample dates(F¼ 7.25; df¼ 8, 24; p< 0.001) for young nymphs (F¼ 16.19; df¼ 8,24; p < 0.001) for older nymphs and (F ¼ 29.67; df ¼ 8, 24;p < 0.001) for adults. There was no significant time by treatmentinteraction for adults (F ¼ 1.24; df ¼ 8.27; p ¼ 0.314) so the overalltreatment means are shown in Table 2. There was no evidence ofoverall time differences (F ¼ 0.22; df ¼ 1, 27; p ¼ 0.644). There was

Table 3Square root transformed means of L. rugulipennis numbers recorded over the firsttwo post-treatment sample dates on strawberry in 2009. Back-transformed means(counts) are given below in parentheses.

Treatment L. rugulipennis stage

Instars 1e2 Instars 3e5 Adults Total

Table 2Overall mean square root transformed numbers of the target stages of L. rugulipennis recorded in the three experiments on weeds in 2008. Back-transformed means (counts)are given in parentheses.

Treatment Experiment 1 Experiment 2 Experiment 3 Mean Rank

Instars 1e2 Instars 3e5 Adults

Mean Rank Mean Rank Mean Rank

Bifenthrin 0.000 (0.00) 1 0.125 (0.02) 1.5 0.125 (0.02) 2 1.5Thiacloprid 2.024 (4.10) 5 3.907 (15.26) 4 0.729 (0.53) 3 4.0Thiacloprid þ surfactant 1.446 (2.09) 3 3.634 (13.21) 3 0.985 (0.97) 4 3.3Acetamiprid 1.937 (3.75) 4 3.995 (15.96) 5 1.047 (1.10) 5 4.7Flonicamid 2.758 (7.61) 6 4.273 (18.26) 6 2.231 (4.98) 7 6.3Lambda cyhalothrin 0.141 (0.02) 2 0.125 (0.02) 1.5 0.000 (0.00) 1 1.5Indoxacarb 3.128 (9.78) 7 5.663 (32.07) 8 2.208 (4.88) 6 7.0Etoxazole 4.077 (16.62) 8 5.649 (31.91) 7 2.846 (8.10) 8 7.7Untreated 4.120 (16.97) 9 5.861 (34.35) 9 3.294 (10.85) 9 9.0

p <0.001 <0.001 <0.001F 57.94 33.74 29.67SED 0.2797 0.5331 0.3081df 8, 32 8, 24 8, 24LSD (p ¼ 0.05) 0.570 1.100 0.636

J. Fitzgerald, C. Jay / Crop Protection 30 (2011) 1178e1183 1181

also no significant time by treatment interaction for 1st and 2ndinstar (F ¼ 0.50; df ¼ 8, 27; p ¼ 0.845) and 3rd and 4th instarnymphs (F¼ 0.70; df¼ 8,27; p¼ 0.688), nor overall time differences(F ¼ 0.48; df ¼ 1,27; p ¼ 0.493 and F ¼ 1.03; df ¼ 1, 27; p ¼ 0.319),but there was a significant time by treatment interaction for 5thinstar nymphs (F ¼ 3.70; df ¼ 8 and 27; p ¼ 0.005), with numberssignificantly lower 5 DAT compared with 1 DAT for the flonicamidtreatments, possibly indicating a slower mode of action of thisproduct on this stage.

Overall results are given in Table 2 showing the results for thetarget group for each experiment, along with the ranking of themeans. There was a consistent pattern of results, with bifenthrinand lambda cyhalothrin giving the greatest reductions in numbersof L. rugulipennis of all developmental stages (lowest means)throughout. This is reflected in their joint mean ranking of 1.5. Theuntreated control had consistently the highest numbers ofL. rugulipennis, with the etoxazole treatment never differingsignificantly from the control. Although flonicamid and indoxacarbdid give significant reductions in numbers compared to the control(for all except indoxacarb in experiment 2 targeting the 3rde5thinstar nymphs), numbers were significantly higher than in thebifenthrin, thiacloprid, thiacloprid þ surfactant, acetamiprid andlambda cyhalothrin treatments for both experiments 1 and 3. Inexperiment 2, treatments appeared to be generally less effective atreducing numbers of L. rugulipennis than in the other two trials,except for the most effective treatments, bifenthrin and lambdacyhalothrin. This may suggest that the compounds tested were notas effective against 3rde5th instar nymphs as young nymphs andadults.

Bifenthrin 0.10 0.00 0.10 0.20(0.01) (0.01) (0.01) (0.04)

Thiacloprid 2.21 3.01 0.83 4.09(4.88) (9.06) (0.69) (16.73)

Thiacloprid þ surfactant 1.56 2.83 0.70 3.51(2.43) (8.01) (0.49) (12.32)

Acetamiprid 2.05 2.94 0.94 3.90(4.20) (8.64) (0.88) (15.21)

Untreated 2.09 3.00 0.62 3.96(4.37) (9.00) (0.38) (15.68)

p <0.001 <0.001 0.109 <0.001F 14.98 57.32 2.16 58.19SED (4, 21df)a 0.320 0.250 0.313 0.308LSD (p ¼ 0.05)a 0.665 0.519 0.651 0.641

a For comparisons between all treatments except ‘thiacloprid þ surfactant’whichhas double replication; SEDs and LSDs for comparisons with this treatment need tobe multiplied by 0.866.

3.2. 2009 Experiment

Analysis of the pre-treatment samples showed no differencesbetween treatment plots, indicating that numbers were similaracross the planting. In the analysis of the results, the use of pre-treatment numbers as a covariate was not significant so resultsare presented here without covariate adjustment. Since the post-treatment analysis showed that there was no interaction betweentime of sampling and numbers of L. rugulipennis in the differenttreatments (F¼ 1.01; df¼ 4, 25; p¼ 0.419 for first two sample datesand F ¼ 0.30; df ¼ 5,24; p¼ 0.907 for second two sample dates), i.e.although numbers changed over time these changes followed thesame trend on the different sample dates regardless of treatment,overall analysis of numbers recorded in the first two and the second

two samples (i.e. before and after the second application ofthiacloprid þ surfactant) are presented in Tables 3 and 4.

Results in Table 3 show that in the samples taken 3 and 9 daysafter the initial treatment applications, 1st and 2nd instarL. rugulipennis were significantly lower than the control only in thebifenthrin treatment. However, there was an indication thatnumbers in the thiaclopridþ surfactant treatment were lower thanin the thiacloprid alone treatment. For the older nymphs and adultsonly the bifenthrin treatment had any significant effect onnumbers. Looking at totals of all stages, only the bifenthrin treat-ment was significantly different from the control. For the individualstages the overall time effect was significant (F ¼ 15.74; df ¼ 1, 25;p < 0.001), for 1st and 2nd instars, (F ¼ 6.76; df ¼ 1, 25; p ¼ 0.015)for older nymphs and (F¼ 8.29; df¼ 1, 25; p¼ 0.008) for adults; forthe nymphs counts were higher for the later time but for adults theearlier time had higher counts with the totals showing no timedifferences (F ¼ 0.11; df ¼ 1,25; p ¼ 0.738).

Results in Table 4 show that 1st and 2nd instar nymphs weresignificantly different from the control only in the bifenthrintreatment in samples taken 3 and 9 days after the secondthiacloprid þ surfactant application on 11 August. There was alsoa decreasing trend in numbers in the thiacloprid þ surfactant

Table 4Square root transformedmeans of L. rugulipennis numbers recorded over the secondtwo post-treatment sample dates on strawberry in 2009. Back-transformed means(counts) are given below in parentheses.

Treatment L. rugulipennis stage

Instars 1e2 Instars 3e5 Adults Total

Bifenthrin 0.96 2.35 1.57 3.15(0.92) (5.52) (2.46) (9.92)

Thiacloprid 2.93 4.15 2.25 5.66(8.58) (17.22) (5.06) (32.04)

Thiacloprid þ surfactant 2.78 3.69 1.79 5.03(7.73) (13.62) (3.20) (25.30)

Thiacloprid þ surfactant � 2 2.38 3.03 2.21 4.55(5.66) (9.18) (4.88) (20.70)

Acetamiprid 2.76 3.71 2.26 5.21(7.62) (13.76) (5.11) (27.14)

Untreated 2.51 3.53 2.28 4.97(6.30) (12.46) (5.20) (24.40)

p <0.001 <0.001 0.135 <0.001F 11.90 15.82 1.92 18.43SED (5, 20df) 0.298 0.225 0.309 0.286LSD (p ¼ 0.05) 0.621 0.469 0.645 0.598

J. Fitzgerald, C. Jay / Crop Protection 30 (2011) 1178e11831182

applied once and then this treatment applied twice; this decreasewas not quite strong enough for standard statistical significance.For the older nymphs results were similar to those of instars 1 and 2except that thiaclopridþ surfactant applied twice gave a significantreduction in numbers when compared to thiacloprid alone. Onlybifenthrin significantly reduced numbers of L. rugulipennis adults.Looking at totals of all stages, only numbers in the bifenthrintreatment were significantly different from the control. However,there was evidence of numbers in the thiacloprid treatment beingsignificantly higher than in the thiacloprid þ surfactant appliedonce, which was significantly higher than this treatment appliedtwice. For the individual stages the overall time effect was notsignificant for nymphs (F ¼ 2.20; df ¼ 1, 24; p ¼ 0.151 for youngnymphs and F ¼ 1.07; df ¼ 1, 24; p ¼ 0.311 for older nymphs) butwas for adults (F¼ 30.78; df¼ 1, 24; p< 0.001) and totals (F¼ 4.33;df ¼ 1, 24; p ¼ 0.048) with the later time having higher counts.

4. Discussion

Several reports have highlighted insecticides that have beenshown to be effective against related capsid species on strawberryor other crops in other countries, but many of these are unsuitablefor use within IPM programmes. For example Zhang et al. (2009)tested a wide range of compounds in laboratory bioassays andshowed that malathion, chlorpyrifos, bifenthrin, methomyl, endo-sulfan and fipronil were highly toxic to Lygus lucorum Meyer-Dur.Similarly Thompson et al. (2009) reported the effectiveness ofthiamethoxam and fenpropathrin against Lygus species in straw-berry in California. In bioassays to determine if resistance wasdeveloping to selected insecticides in populations of L. lineolarisSnodgrass et al. (2008) reported that thiamethoxam and imida-cloprid were effective against populations of this pest in USA.However, Bostanian et al. (2005) showed that the residual activityof thiamethoxam, thiacloprid and acetamiprid to L. lineolaris wasvery short lived in orchards.

Despite the importance of L. rugulipennis as a pest of severaldifferent crops, there are few recent published reports of tests ofefficacy of insecticides against this pest. Cross (2004) outlined thecontrol strategies for the pest available at that time in the UK; themost effective compounds were pyrethroids and chlorpyrifos.Pansa et al. (2008) obtained variable results in laboratory and fieldexperiments in Italy; in the field experiments spinosad and

thiacloprid gave less than 50% mortality of adults and indoxacarbgave 100% mortality whereas it had only given 7% mortality ina laboratory bioassay. Also Fitzgerald (2004) showed that applica-tions of thiacloprid significantly reduced populations ofL. rugulipennis on everbearer strawberries. The current experi-ments, undertaken over two years, showed that of the compoundstested the pyrethroids gave the greatest reductions overall innumbers of L. rugulipennis of all developmental stages; thesecompounds were used in the experiments as a standard toxicinsecticide and should be avoided in strawberry plantations thatare using IPM strategies. In the experiment in 2009 on strawberry,numbers of L. rugulipennis in the bifenthrin treatment were stillsignificantly lower than in any other treatment 23 days afterapplication, highlighting the persistence of this product. In theexperiments targeting the different life stages of L. rugulipennis in2008 to determine if timing pesticide applications with regard tothe life stages present could improve control, therewas a consistentpattern of results with no apparent differential effects of thecompounds tested. Thus there was no evidence to suggest thattiming application of the tested insecticides against specific lifestages would significantly improve pest control. This contradictsthe results of Fitzgerald (2004) where in a replicated field experi-ment thiacloprid gave a significant reduction of L. rugulipennisnymphs, but not of adults, and also significantly reduced fruitdamage. Overall the 2008 experiments showed that etoxazole hadno effect on L. rugulipennis and that although flonicamid andindoxacarb significantly reduced populations they were not aseffective as thiacloprid, either with or without a surfactant, oracetamiprid. The first post-treatment samples in these experimentswere taken soon after pesticide application to minimise thepotential confounding effects of movement of L. rugulipennisbetween the relatively small treated plots. It is possible thata greater effect may have been detected with some of theseinsecticides if they had been applied to larger plots. Furtherresearch is needed to test this.

In the 2009 experiment on strawberry, thiacloprid þ surfactantapplied twice was more effective than this treatment applied once,which in turn was more effective than thiacloprid alone. Surfac-tants can increase the efficacy of insecticides by spreading themover the plant surface (e.g. Zhang et al., 2006) and increasing thedose of insecticide per unit area; the use of surfactants has recentlybeen shown to increase the efficacy of several acaricides against thephytophagous mite P. pallidus on strawberry (Fountain et al., 2010).Thus a programme of applications of thiacloprid þ surfactant maybe an effective strategy for reducing L. rugulipennis populations.Further work is needed to determine the effects of other surfactantson L. rugulipennis control. Earlier field experiments (Fitzgerald,2004) indicated that applications of acetamiprid and thiaclopridhad little effect on numbers of naturally occurring beneficialspecies in the plantation so could be used within IPM programmes.

It is not clear why the tested compounds were less effective in2009 than in 2008, but it is possible that on the waxy strawberryplants coverage was not as good as on the weeds in 2008 evenwhen a surfactant was used, or that spray penetration was poorerin the denser strawberry foliage.

With few selective chemicals available showing efficacy againstL. rugulipennis it is apparent that new methods to control thisdamaging pest need to be developed. Several areas are currentlybeing explored. In a survey in Sweden Ramert et al. (2005) iden-tified several species of Tachinid and Braconid parasitoids attackingL. rugulipennis, and in the USA methods are being developed to useparasitoids to control the pest (Pickett et al., 2009). However, in theUK it is only permitted to release native species of predator orparasitoid as biocontrol agents, so more work is needed to identifythe parasitoid complex present before this strategy could be

J. Fitzgerald, C. Jay / Crop Protection 30 (2011) 1178e1183 1183

developed here (e.g. Gariepy et al., 2008). An alternative is todevelop microbial insecticides for control (e.g. Jacobson, 2002;Sabbahi et al., 2008), but conditions within poly tunnels may beunsuitable for their growth. A more promising approach is todevelop methods that are based on manipulating the behaviour ofthe pest, using trap crops (e.g. Swezey et al., 2007; Pansa andTavella, 2009) and/or semiochemicals (e.g. Glinwood et al., 2003;Innocenzi et al., 2004, 2005) to attract the pest away from thecrop. Work in this area is ongoing at EMR.

Acknowledgements

This project was funded by the UK Agriculture and HorticultureDevelopment Board. We thank Mike Easterbrook and Adrian Harrisfor technical support and Gillian Arnold for statistical analysis.

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