Impact of Plant Growth-Promoting Rhizobacteria and Natural Enemies on Myzus persicae (Hemiptera: Aphididae) Infestations in Pepper

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1 Impct of Plnt Growth-Promoting Rhizocteri nd Nturl Enemies on Myzus persice (Hemipter: Aphidide) Infesttions in Pepper Author(s): Croline Boutrd-Hunt, Christine D. Smrt, Jennifer Thler, nd Brin A. Nult Source: Journl of Economic Entomology, 102(6): Pulished By: Entomologicl Society of Americ DOI: URL: BioOne ( is nonprofit, online ggregtion of core reserch in the iologicl, ecologicl, nd environmentl sciences. BioOne provides sustinle online pltform for over 170 journls nd ooks pulished y nonprofit societies, ssocitions, museums, institutions, nd presses. Your use of this PDF, the BioOne We site, nd ll posted nd ssocited content indictes your cceptnce of BioOne s Terms of Use, ville t Usge of BioOne content is strictly limited to personl, eductionl, nd non-commercil use. Commercil inquiries or rights nd permissions requests should e directed to the individul pulisher s copyright holder. BioOne sees sustinle scholrly pulishing s n inherently collortive enterprise connecting uthors, nonprofit pulishers, cdemic institutions, reserch lirries, nd reserch funders in the common gol of mximizing ccess to criticl reserch.

2 HORTICULTURAL ENTOMOLOGY Impct of Plnt Growth-Promoting Rhizocteri nd Nturl Enemies on Myzus persice (Hemipter: Aphidide) Infesttions in Pepper CAROLINE BOUTARD-HUNT, 1,2 CHRISTINE D. SMART, 3 JENNIFER THALER, 4 AND BRIAN A. NAULT 1 J. Econ. Entomol. 102(6): 2183Ð2191 (2009) ABSTRACT Mngement of green pech phid, Myzus persice (Sulzer) (Hemipter: Aphidide), in ell pepper, Cpsicum nnuum L., ws explored through comintion of plnt growth-promoting rhizocteri (PGPR) nd endemic iologicl control in New York in 2006 nd We hypothesized tht y using PGPR-treted peppers 1) M. persice infesttions would e reduced vi induced resistnce, 2) nturl enemies would e lured to plnts through the elicittion of voltile orgnic compounds, nd 3) yield mount nd qulity would e improved. Pepper seed ws plnted in soil contining the PGPR formultion BioYield or untreted soil. Plnts were trnsplnted to Þeld plots nd then treted with n regimen designed to remove or conserve popultions of nturl enemies. Apterous phids nd nturl enemies were counted weekly on plnts nd pepper fruit were hrvested, grded nd weighed three times. PGPR did not directly or indirectly reduce phid densities in either yer. In 2006, there were more nturl enemies in PGPR-treted plots thn untreted ones, ut this ws proly density-dependent response to phid densities rther thn response of nturl enemies to voltiles from PGPR-treted plnts. For the Þrst hrvest dte in 2006, yield of ll fruit grdes, especilly the premium Fncy Grde, ws 1.7Ð2.3 times greter in PGPR-treted plots thn in untreted plots. However, no differences in yield were oserved for the other two hrvest dtes or overll yield in 2006; no differences in yield mong tretments were detected in Our results suggest tht PGPR will not signiþcntly impct M. persice infesttions or nturl enemy popultions ut could enhnce yield nd qulity of pepper fruit in some yers. KEY WORDS Myzus persice, plnt growth-promoting rhizocteri, pepper, iologicl control Bell pepper, Cpsicum nnuum L., is grown on nerly 120 h (300 cres) in New York nd is vlued t over US$6 million nnully (NASS 2008). The principl rthropod pest of pepper in New York is the Europen corn orer, Ostrini nuillis (Hüner). Brod-spectrum s used to control O. nuillis cn cuse outreks of n importnt secondry pest, the green pech phid, Myzus persice (Sulzer). This common phenomenon occurs when M. persice popultions re resistnt to the pplied (Foster et l. 2000), ut popultions of nturl enemies tht often reduce M. persice infesttions re susceptile. M. persice hs developed resistnce to mny of the mjor pesticide groups, including crmtes, orgnophosphtes, nd pyrethroids (Devonshire nd Moores 1982). M. persice my prthenogeniclly produce up to ten offspring per dy (Estop 1977), which over seson cn led to 22 genertions on summer hosts (Horsfll 1924). This high rte of fecundity nd their propensity 1 Deprtment of Entomology, Cornell University, New York Stte Agriculturl Experiment Sttion, 630 W. North St., Genev, NY Corresponding uthor, e-mil: c239@cornell.edu. 3 Deprtment of Plnt Pthology nd Plnt-Microe Biology, Cornell University, New York Stte Agriculturl Experiment Sttion, 630 W. North St., Genev, NY Deprtment of Entomology, Cornell University, Ithc, NY for developing resistnce to s mkes M. persice n importnt pest to mnge with tctics other thn s. Plnt growth-promoting rhizocteri (PGPR) cn enhnce plntõs ility to defend itself from insects nd pthogens y eliciting defensive responses, lso known s induced resistnce (Kloepper et l. 2004). Induced resistnce is the production of defensive compounds in response to ttck y pthogen or herivory. Induced resistnce my e grouped into two ctegories, systemic cquired resistnce (SAR) nd induced systemic resistnce (ISR), depending on how the resistnce ws triggered nd which chemicl pthwys re ctivted. ISR is triggered in response to herivory, drought, certin pthogens, nd mechnicl wounding. ISR is medited through the ctivtion of the jsmonte pthwy (Thler et l. 2001). SAR my e triggered y pthogens nd some insects, such s phids (for review, see vn Loon et l. 1998) nd is medited through the ctivtion of the slicylic cid pthwy. Stimultion of either or oth pthwys cn directly impct phids y reducing Þtness, fecundity, nd feeding (Cooper et l. 2005, Boughton et l. 2006). PGPR lso could indirectly reduce phid popultions y ttrcting nturl enemies to plnts. The elicittion of voltile orgnic compounds (VOC), which /09/2183Ð2191$04.00/ Entomologicl Society of Americ

3 2184 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 102, no. 6 occurs when plnt defense pthwys re triggered y PGPR, hs een shown to ttrct nturl enemies (De Mores et l. 1998, McGregor nd Gillespie 2004, Girling et l. 2006). For exmple, mycorrhizl interctions within the rhizosphere signiþcntly increse forging in the phid prsitoid Aphidius ervi Hlidy (Guerrieri et l. 2004). Becuse PGPR-relted VOCs ct y triggering rod rnge of defensive rections, oth direct nd indirect, the development of resistnce y pests is unlikely. Perhps PGPR pplied to pepper plnts could directly nd indirectly regulte M. persice infesttions y reducing their Þtness, fecundity, nd feeding, s well s ttrcting nturl enemies to increse phid mortlity. Hermn et l. (2008) recently reported tht the PGPR formultion, BioYield, hd no sttisticlly signiþcnt impct on M. persice densities in pepper in New York. However, the seson totl numers of M. persice in BioYield-treted plots were 49 nd 41% lower thn in untreted plots in 2003 nd 2004, respectively. In tht study, nturl enemies were reduced from test plots y using multiple pplictions of the rod-spectrum pyrethroid esfenvlerte. The purpose of those pplictions ws to mnipulte the system to promote increses in M. persice popultions in the Þeld. M. persice popultions were considered high in 2003 ut low in 2004 nd virtully nonexistent in We expnded upon this previous study y exmining the direct impct of BioYield on infesttions of M. persice s well s the impct of nturlly occurring predtors nd prsitoids on M. persice infesttions. The gol of this study ws to exmine the utility of PGPR, in comintion with endemic nturl enemies for controlling M. persice nd for improving pepper yield nd qulity. We hypothesized tht y using PGPR-treted peppers 1) M. persice infesttions would e reduced vi induced resistnce, 2) nturl enemies would e lured to plnts through the elicittion of voltile orgnic compounds, nd (3) yield mount nd qulity would e improved. Mterils nd Methods Plnting nd PGPR Inocultion. Bell pepper seeds ÔCmelotÕ were plnted in 128-cell ßts in Cornell Mix soil-less plnting mix, prepred with 4Ð1Ð1 rtio with perlite nd vermiculite. In ll studies, the PGPR formultion BioYield (Byer CropScience, Reserch Tringle Prk, NC) consisted of colony-forming units (CFUs) of Penocillus mcerns GB122 nd Bcillus myloliquefciens GB99 per liter of plnting mix. For ech ßt, 1.2 g of BioYield ws incorported into the plnting mix y using soil mixer efore seeds were plnted. After seeding, the pepper ßts were plced in greenhouse (photoperiod of 16:8 [L:D] h) t the New York Stte Agriculturl Experiment Sttion in Genev, NY, until plnts were 8 wk old. The peppers were moved into outdoor cold frmes for minimum of week efore trnsplnting. Peppers were trnsplnted during the weeks of 12 June nd 4 July 2006 nd during the sme week of 11 Tle 1. Tretments exmined for their impct on nturlly occurring popultions of green pech phid nd nturl enemies in ell pepper in New York in 2006 nd 2007 Fctor 1 (PGPR) Fctor 2 () Intended impct on phids Intended impct on nturl enemies No PGPR No None None No PGPR Pymetrozine Reduce None (FulÞll) No PGPR Esfenvlerte Increse Reduce (Asn) PGPR No None Increse PGPR Pymetrozine Reduce Increse (FulÞll) PGPR Esfenvlerte (Asn) Slight increse Reduce June Field plots consisted of six rows nd four rows in 2006 nd 2007, respectively. Rows were 7.6 m in length nd spced 0.9 m prt. Plnts were spced t 0.3-m intervls within rows. In 2006 nd 2007, plots were distriuted cross three Þelds tht were seprted y 0.5Ð2 km. Within ech Þeld, plots were seprted from ech other y minimum of 15.2 m in 2006 nd 7.6 m in All plots within repliction were locted in the sme Þeld. Drip irrigtion ws used to hydrte ll plots in 2007, ut no irrigtion ws necessry in Supplementl fertiliztion ws lso pplied following stndrd recommendtions (Reiners nd Petzoldt 2008). Insecticides. Insecticides were selected to mnipulte popultions of M. persice nd nturl enemies to test our hypotheses (Tle 1). The rod-spectrum pyrethroid esfenvlerte (Asn XL, DuPont, Wilmington, DE) ws used t rte of 0.3 liters/h to reduce nturl enemies in one third of the tretments. Esfenvlerte hs moderte toxicity to predtors nd high toxicity to prsitoids (University of Cliforni 2005). The other product ws the phicide pymetrozine (FulÞll, Syngent Crop Protection, Greensoro, NC), which ws used t rte of 0.2 kg/h to reduce phids without ffecting nturl enemy popultions in the plots. Finlly, there were plots to which no s were pplied. All tretments were pplied using ckpck spryer nd three-nozzle oom delivering spry volume of 271 liters/h t 276 kp. All s were mixed with 0.5% (vol:vol) of Silwet surfctnt. Tretments were initilly pplied when the M. persice popultion reched threshold of one phid per lef. Additionl pplictions were mde 3Ð4 wk fter the Þrst spry. In 2006, tretment plots were spryed ccordingly with esfenvlerte nd pymetrozine twice during the seson, on 21 July nd 17 August. In 2007, plots were spryed with the tretments three times: 11 July, 9 August, nd 9 Septemer. Effect of PGPR on Aphids nd Nturl Enemy Densities. We hypothesized tht if PGPR triggered direct negtive effect on phid popultions, our est opportunity to oserve this response in the Þeld would e in plots treted with esfenvlerte, which would remove nturl enemies tht often regulte

4 Decemer 2009 BOUTARD-HUNT ET AL.: MANAGEMENT OF GREEN PEACH APHID IN PEPPER 2185 phid popultions. Thus, we expected to oserve lower phid densities in PGPR plots treted with esfenvlerte thn in plots without PGPR treted with esfenvlerte (Tle 1). There were six tretments in this 2-yr project. The experiment ws designed s 2 y 3 fctoril with PGPR s the Þrst fctor (PGPR versus no PGPR) nd s the second fctor (no, pymetrozine nd esfenvlerte). All tretments were rrnged in rndomized complete lock design nd replicted Þve times in 2006 nd eight times in M. persice nd nturl enemies were surveyed in plots nerly every week from 17 July to 27 Septemer in 2006 nd from 3 July to 11 Octoer in In 2006, phids nd nturl enemies were counted from 30 plnts rndomly chosen from ech of the two middle rows. Becuse no signiþcnt difference in phid numers per plnt ws found etween counting phids on 30 nd 15 plnts, smple size ws reduced to 15 plnts in Three leves were rndomly chosen from the middle cnopy of ech plnt, nd the numer of pterous dults nd immtures ws recorded. We lso hypothesized tht nturl enemies would e higher in PGPR-treted plots thn in those not treted with PGPR ecuse they would e ttrcted to VOCs. Testing this ide required the use of selective such s pymetrozine tht would 1) reduce phid popultions to eliminte the possiility of positive density-dependent response y nturl enemy popultions nd 2) reduce phid popultions in mnner tht would not negtively impct nturl enemies. Nturl enemies tht were oserved in our study were recorded to the fmily level nd included Anthocoride, Chrysopide, Coccinellide, Hemeroiide, Cecidomyide, nd Syrphide. Prsitized phids (mummies) were recorded s n indictor of the reltive undnce of hymenoptern prsitoids. No fungl epizootics were oserved during this study. Yield. We hypothesized tht fruit yield or lrger fruit grdes (e.g., Fncy grde) or oth would e greter in PGPR-treted plots thn in non-pgprð treted plots. Peppers were hrvested nd grded t three points during ech seson. In 2006, peppers were hrvested on 24 August, 21 Septemer, nd 3 Octoer. In 2007, peppers were hrvested on 29 August, 14 Septemer, nd 10 Octoer. Peppers were divided into the three grdes s deþned y the USDA nd used for ntionl mrket orders (USDA 2005). Fncy grde peppers re deþned s fruit with 7.62-cm dimeter nd 8.90-cm length; U.S. no. 1 grde fruit must hve dimeter etween 6.35 nd 7.62 cm, nd length 6.35 cm; nd U.S. no. 2 grde fruit ws considered unmrketle or s culls in our study. Fncy grde, no. 2 grde nd totl yield cross ll grdes were nlyzed. The no. 2 grde peppers were nlyzed seprtely to ensure tht ny differences in yield etween the tretments were due to incresed mrketle yields. An increse in no. 2 grde peppers, which would need to e culled, would increse picking costs, reducing proþt. Yield differences solely ttriutle to our tretments were of primry interest. Therefore, we did not exclude fruit with physicl ßws, Europen corn orer injury or disese, ll of which were uncommon in our study. Sttisticl Anlyses. The effects of BioYield,, smpling dte, nd their interctions with insect undnce were exmined y repeted mesures nlysis of vrince (ANOVA) using the Proc Mixed procedure in SAS 9.1 (SAS Institute 2003). The vriles PGPR,, nd smpling dte were considered Þxed nd unstructured in our models. First-order utoregressive covrince structures were used to model covrince etween tretments nd smpling dtes y choosing comintion of AkikeÕs informtion criterion, which evlutes whether the model used est explins the dt, while minimizing free prmeters in the model. The expecttion ws tht correltions would e greter for counts tken on dtes tht were closer together. For nturl enemy dt, the model ws run s descried ove, then rerun with phid dt included s covrite to ccount for ny numericl effect. Repliction ws considered rndom effect in the model. Independent sttisticl nlyses were performed on ech nturl enemy group, ut ecuse trends were similr for ech group, dt were pooled into single ctegory clled totl nturl enemies. Totl mrketle fruit yield nd yield seprted y grde were oth nlyzed s two-wy ANOVA. Fruit hrvested from ech plot row ws verged to provide the verge yield per row for the plot. In 2006, lte plnting due to wether conditions ffected plnt growth in two of the Þve replictes, which then were excluded from the nlysis (n 3). All eight replictes were included in the 2007 nlysis. Mens were compred using the Proc Mixed procedure in SAS 9.1. Some dt were trnsformed using log 10 (x 1) trnsformtion to normlize dt efore nlysis, ut only untrnsformed dt re presented. Nturl enemy, prsitoid, nd predtor densities were compred with phid densities using PersonÕs productmoment correltion (P 0.05). Results Wether Conditions. Wether conditions vried sustntilly etween 2006 nd 2007, prticulrly in June, when most peppers were trnsplnted into the Þeld. The 2006 verge temperture for June ws 18.9 C, pproximtely equl to the 10-yr verge. Rinfll in June 2006 ws 12.7 cm, 2.9 cm ove verge. Precipittion in July nd Septemer ws lso ove verge. Extended periods of rinfll re stressful for peppers nd my reduce growth (Jett 2006). In 2007, Genev experienced the second wrmest June in the pst 30 yr (Ntionl Wether Service, The verge dily temperture ws 19.9 C, which ws 1 C ove the 10-yr verge. Rinfll in June 2007 ws 5.33 cm, which ws 5.08 cm less thn verge. Due to the dry conditions tht persisted throughout the 2007 summer, drip irrigtion ws used for the entire Þeld seson. Irrigtion signiþcntly increses the vigor nd yield of ell pepper (Cost nd Ginquinto 2002).

5 2186 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 102, no. 6 A Aphids per lef B Aphids per Lef pplied pplied Julin dte pplied pplied Julin Dte pplied c no pymetrozine esfenvlerte no pymetrozine esfevlerte Fig. 1. Effect of on M. persice densities on ell pepper through the seson in Genev, NY, in 2006 (A) nd 2007 (B). Dtes on which signiþcnt differences occurred mong tretments re mrked with letters. Tretment mens shring the sme letter re not signiþcntly different (P 0.05). Aphid Density. Aphid densities differed sustntilly etween the 2 yr (Fig. 1). In 2006, there ws n overll verge of 2.7 phids per lef, wheres the verge ws 0.3 phids per lef in PGPR hd no effect on phid density in either 2006 or 2007 (Tle 2). Aphid density ws signiþcntly ffected y s well s y n interction etween nd dte in oth 2006 nd 2007 (Tle 2). Plots treted with esfenvlerte hd signiþcntly more phids thn those in untreted plots nd those treted with Tle 2. Significnce of PGPR,, nd their interction on M. persice on ell pepper through time in Genev, NY, in 2006 nd 2007 Source df F P 2006 PGPR Insecticide PGPR Dte PGPR dte Insecticide dte PGPR dte PGPR Insecticide Dte PGPR PGPR dte Insecticide dte PGPR dte pymetrozine, especilly fter Julin dte 229 in 2006 (Fig. 1A) nd fter Julin dte 249 in 2007 (Fig. 1B). This difference ws most drmtic in 2006 when there ws seson verge of phids per lef in esfenvlerte-treted plots nd only phids per lef in the untreted control (Fig. 1A). The verge numer of phids in plots treted with pymetrozine did not differ from the numer in untreted plots in 2006 (Fig. 1A) nd 2007 (Fig. 1B). Aphid densities were not impcted y n interction etween PGPR nd in either 2006 or 2007 (Tle 2). We predicted tht if PGPR hd negtive effect on phid densities, we would oserve lower phid densities in PGPR plots treted with esfenvlerte thn in plots without PGPR treted with esfenvlerte (i.e., signiþcnt PGPR interction). However, the interction did not exist nd the opposite ws oserved. Plots treted with oth PGPR nd esfenvlerte hd seson verge of phids per lef, wheres plots treted with esfenvlerte lone hd n verge of phids per lef. Nturl Enemies. More nturl enemies were oserved in plots in 2006 thn in 2007 (Fig. 2). Yet, the proportion of ech group of nturl enemies reltive to the totl numer of nturl enemies encountered ws reltively similr etween yers (Fig. 2). Coccinellids nd prsitoids were the most dominnt groups oserved.

6 Decemer 2009 BOUTARD-HUNT ET AL.: MANAGEMENT OF GREEN PEACH APHID IN PEPPER 2187 A Hymenopter (prsitoids) Coccinellide (multiple spp.) Neuropter (multiple spp.) Dipter (multiple spp.) Anthocorcide B Hymenopter (prsitoids) Coccinellide (multiple spp.) Neuropter (multiple spp.) Dipter (multiple spp.) Anthocorcide Fig. 2. Nturl enemies of M. persice smpled on plnts cross ll tretments in 2006 (A) nd 2007 (B) nd their reltive undnce. PGPR hd signiþcnt effect on nturl enemies in 2006, ut not in 2007 (Tle 3). Overll, 17% more nturl enemies were oserved in PGPR-treted plots thn in those not treted with PGPR. Insecticide lso Tle 3. Significnce of PGPR,, nd their interctions on totl nturl enemy density through time, in Genev, NY, in 2006 nd 2007 Source df Including phid Norml density s covrite F P F P 2006 PGPR Insecticide PGPR Dte PGPR dte Insecticide dte PGPR dte Aphid density PGPR Insecticide PGPR Dte PGPR dte Insecticide dte PGPR dte impcted nturl enemy densities in 2006, ut not in 2007 (Tle 3). Over the entire 2006 seson, the verge numer of nturl enemies in esfenvlertetreted plots (174 24) ws signiþcntly greter thn the verge numer in pymetrozine-treted (27 4) or untreted plots (51 6.8). In ddition, more nturl enemies were oserved in esfenvlerte-treted PGPR plots thn in esfenvlerte-treted plots tht did not receive PGPR (i.e., interction etween PGPR nd ) (Tle 3; Fig. 3). We did not nticipte encountering more nturl enemies in esfenvlerte-treted plots thn in the other tretments ecuse the purpose of using esfenvlerte ws to eliminte nturl enemies. This ws not successful lter in the seson nd we suspected tht the high numer of nturl enemies in esfenvlertetreted plots ws positive density-dependent popultion response to the high numer of phids in these plots. Thus, when the ANOVA model included phid density s covrite in the nlysis, neither the PGPR min effect nor the interction etween PGPR nd were signiþcnt. Nturl enemy densities in oth PGPR-treted (r 2 0.7, df 9, P 0.001) nd untreted plots (r 2 0.4, df 9, P 0.001) were positively correlted with the numer of phids per lef. These results indicted tht the higher numer of nturl enemies in the plots treted with PGPR nd esfenvlerte ws density-dependent numericl re-

7 2188 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 102, no seson totl verge nturl enemies per plot c 0 untreted, no (1) untreted, pymetrozine (2) untreted, PGPR, no esfenvlerte (3) (4) tretment PGPR, pymetrozine (5) PGPR, esfenvlerte (6) Fig. 3. Effect of PGPR nd on nturl enemy densities in Mens SEM shring the sme letter re not signiþcntly different (P 0.05). sponse to phid popultions within the plots, rther thn response of nturl enemies to VOCs. The impct of on nturl enemy densities through time ws similr to the impct tht hd on phid densities through time in 2006 (Tle 3; Fig. 4). More nturl enemies were oserved in esfenvlerte-treted plots thn in the other tretments fter Julin dte 229 (Fig. 4), nd no differences existed etween pymetrozine nd untreted plots. Yield. In 2006, PGPR hd signiþcnt positive effect on oth fncy grde (Tle 4) nd yield of ll-grdes in the Þrst hrvest (Tle 5). The per-row verge yields from the Þrst hrvest of Fncy grde peppers were nd kg in untreted nd PGPR-treted plots, respectively (Fig. 5). For ll grdes, PGPR-treted plots verged kg per row, wheres the verge ws only kg per row in the untreted plots. Neither nor PGPR interction hd n effect on Þrst hrvest yield (Tles 4 nd 5). For the second, third, nd overll hrvest yields, no signiþcnt differences were seen etween PGPR-treted plots nd untreted plots in fncy grde (Tle 4) nd ll grde ctegories (Tle 5). In 2007, there were no signiþcnt interctions etween the vriles PGPR, nd yield (Tles 4 nd 5). Similrly, there ws no signiþcnt effect of or signiþcnt PGR y interction tht ws iologiclly relevnt. Discussion The PGPR formultion, BioYield, hd no impct on M. persice popultions in pepper. This result ws consistent cross yers tht vried sustntilly in oth phid pressure nd environmentl conditions. We hypothesized tht if PGPR triggered direct negtive effect on phid popultions, our est opportunity to oserve this response would e in plots treted with esfenvlerte, which would remove nturl enemies nd llow phid popultions to rech higher levels. This pproch successfully incresed phid popultions, ut nturl enemy popultions responded to the phid increses in positive density-dependent mn- verge numer of nturl enemies per plot pplied pplied Julin dte no pymetrozine esfenvlerte Fig. 4. Effect of on nturl enemy densities of M. persice over the 2006 seson. Dtes on which signiþcnt differences occurred etween tretments re mrked with letter. Mens shring the sme letter etween tretment within dte re not signiþcnt (P 0.05).

8 Decemer 2009 BOUTARD-HUNT ET AL.: MANAGEMENT OF GREEN PEACH APHID IN PEPPER 2189 Tle 4. Significnce of PGPR,, nd their interctions on fncy grde pepper yield cross ll three hrvests nd totl yield in Genev, NY Sources of vrition df Hrvest 1 Hrvest 2 Hrvest 3 Totl F P F P F P F P 2006 PGPR Insecticide PGPR PGPR Insecticide PGPR ner. Consequently, we were not le to compre high phid popultion densities in PGPR-treted nd nontreted plots in the sence of nturl enemies. Nonetheless, our results re identicl to those reported y Hermn et l. (2008), who filed to detect signiþcnt effect of BioYield on M. persice densities in ell pepper in New York over 2 yr. In their study, test plots lso were treted with multiple pplictions of esfenvlerte to increse phid popultions. Comining our results with those presented in Hermn et l. (2008), there were four of 4 yr in which PGPR ws not shown to reduce phid popultions. Thus, our Þrst hypothesisñfewer phids would estlish in PGPR plots compred with untreted plotsñws not sustntited. Direct defenses triggered y PGPR or other elicitors hve een shown to cuse direct ntixenotic nd ntiiotic defenses (Zehnder et l. 2001). Potto phids, Mcrosiphum euphorie (Thoms), tht were fed tomto in the lortory in which the jsmonic cid pthwy hd een rtiþcilly triggered, produced fewer offspring nd hd fewer offspring survive compred with the control (Cooper nd Goggin 2005). If such response occurred in pepper in our study, the difference ws too smll to detect under Þeld conditions nd likely not of prcticl vlue for phid mngement. Overll phid popultion levels in our study were opposite of wht would e expected given the wether conditions. Previous reserch hs found tht M. persice migrtion nd densities re positively correlted with temperture nd hve negtive correltion with rinfll (Cocu et l. 2005, Kuroli nd Lntos 2006). Yet, we oserved higher M. persice popultion levels in 2006, which ws cool nd wet, thn in 2007, which ws hot nd dry. An exception to the 2007 wether pttern occurred in June, when 3 cm of rin fell in 24 h. Perhps this single rin event reduced initil M. persice popultions nd they never recovered. Nturl enemy densities were not impcted y PGPR. Although densities of nturl enemies were signiþcntly higher in plots treted with PGPR thn in those not treted with PGPR in 2006, we demonstrted tht these results were cused y positive densitydependent response to high phid densities. In 2007, when phid pressure ws similr cross ll tretments, no signiþcnt differences in nturl enemy densities were seen etween PGPR nd untreted plots. Thus, there ws no evidence supporting our hypothesis tht PGPR triggered the plntsõ indirect defenses to ttrct higher levels of nturl enemies. The rpid coloniztion of nturl enemies into pepper plots treted with esfenvlerte lte in the seson my hve een excerted y the reltively smll plot size. The lrge re of fllow lnd surrounding test plots supported nturl enemies tht pprently estlished quickly in plots fter the residul ctivity of the esfenvlerte hd dissipted. Perhps, if this study ws conducted in lrger Þeld plots, we would not hve oserved this phenomenon. Endemic nturl enemies were highly effective in mnging M. persice infesttions in pepper in oth yers. Nturl enemies reduced M. persice popultions to sueconomic threshold levels in ll -free plots. Moreover, nturl enemies provided n equivlent level of M. persice reduction s tht provided y multiple pplictions of pymetrozine. PGPR did not consistently increse pepper fruit yield or grde in either yer of our study. The only increse in fruit yield nd grde in PGPR-treted plots Tle 5. Significnce of PGPR,, nd their interctions on ll grdes of pepper yield cross ll three hrvests nd totl yield in Genev, NY Sources of vrition df Hrvest 1 Hrvest 2 Hrvest 3 Totl F P F P F P F P 2006 PGPR Insecticide PGPR PGPR Insecticide PGPR

9 2190 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 102, no. 6 Fig. 5. Effect of PGPR on Þrst hrvest fncy grde pepper yield for 2006 nd Mens SEM shring the sme letter etween tretments nd within yers re not signiþcntly different (P 0.05). ttriutle to PGPR occurred during the Þrst hrvest in In this cse, fruit yield ws nerly douled in plots treted with PGPR s compred with plots not treted with PGPR. Becuse environmentl conditions were stressful for pepper growth erly in 2006, the use of PGPR my hve een responsile for the increse in yield. The sence of fruit yield increses in our study during lter hrvests in 2006 nd ll hrvests in 2007 indicte tht yield eneþt provided y PGPR will not occur consistently. Thus, we cnnot conclude tht PGPR will lwys enhnce yield or grde of pepper. During the period preceding the Þrst hrvest in 2006, phid pressure ws low (less thn two phids per lef) nd similr etween ll tretments. Thus, it is doutful tht the greter yields in PGPR plots were due to incresed phid tolernce t the time of fruit initition nd development. Murphy et l. (2003) reported tht tomto plnts treted with PGPR were 10 d hed in physiologicl mturity thn control plnts of the sme ge. They lso reported tht PGPRtreted plnts hd signiþcntly greter numer of erly seson uds. Boutrd-Hunt (2008) recently showed tht pepper plnts treted with PGPR hd more uds erly in the plntõs development compred with those not treted with PGPR. Greter fruit yield nd percentge of fncy grde peppers produced in PGPR-treted plots erly in our 2006 study could hve een cused y the production of more erly-seson uds. Further investigtion into the effect of PGPR on the initition of ud development would e useful in elucidting the mechnism ehind erly seson yield increses oserved in this nd other studies. High M. persice pressure cn reduce pepper yield (Reiners nd Petzoldt 2008), ut we did not oserve this in either yer of our study. In 2006, phid densities were much greter in esfenvlerte-treted plots nd exceeded the ction threshold more often thn in those plots spryed with either pymetrozine or were not treted. Yet, fruit yield did not differ mong these tretments. These results re consistent with those reported y Hermn et l. (2008). The sence of pepper fruit yield loss ttriuted to M. persice infesttions suggests tht this pest my not need to e mnged with s in smll plntings of pepper in most yers. Our results indicte tht the primry eneþt of using PGPR in pepper production in New York my e s soil mendment to uffer plnts ginst erly seson stress, rther thn s mngement tctic for M. persice or lure for nturl enemies. The use of PGPR in this regrd my ssure growers tht they will hve erly-seson mrketle pepper yield even if growing conditions re not idel. Acknowledgments We thnk M. Hessney, K. Stright, E. Smith, B. English- Loe, T. Evns, H. Schoonover, nd A. Ospin for ssisting with Þeldwork nd dt collection. We lso thnk F. Vermeylen (Deprtment of Sttistics, Cornell University) for sttisticl consulting. This project ws prtilly supported y Federl Formul Funds. References Cited Blckmn, R. L., nd V. F. Estop Aphids on the worldõs crops: n identiþction nd informtion guide. Wiley, New York. Boughton, A. J., K. Hoover, nd G. W. Felton Impct of chemicl elicitor pplictions on greenhouse tomto plnts nd popultion growth of the green pech phid, Myzus persice. Entomol. Exp. Appl. 120: 175Ð188. Boutrd-Hunt, C Evluting the impct of plntgrowth-promoting-rhizocteri nd nturl enemies on Myzus persice infesttions in pepper. M.S. thesis, Cornell University, Ithc, NY.

10 Decemer 2009 BOUTARD-HUNT ET AL.: MANAGEMENT OF GREEN PEACH APHID IN PEPPER 2191 Cocu, N., R. Hrrington, M.D.A. Rounsevell, S. P. Worner, nd M. Hulée Geogrphicl loction, climte nd lnd use inßuences on the phenology nd numers of the phid, Myzus persice, in Europe. J. Biogeogr. 32: 615Ð632. Cooper, W. R., nd F. L. Goggin Effects of Jsmonteinduced defenses in tomto on the potto phid, Mcrosiphum euphorie. Entomol. Exp. Appl. 115: 107Ð115. Cooper, W. R., L. Ji, nd F. L. Goggin Acquired nd R-gene-medited resistnce ginst the potto phid in tomto. J. Chem. Ecol. 30: 2527Ð2542. Cost, L. D., nd G. Ginquinto Wter stress nd wter tle depth inßuence yield, wter use efþciency, nd nitrogen recovery in ell pepper: lysimeter studies. Aust. J. Agric. Res. 53: 201Ð210. De Mores, C. M., W. J. Lewis, P. W. Pré, H. T. Alorn, nd J. H. Tumlinson Herivore-infested plnts selectively ttrct prsitoids. Nture (Lond.) 393: 570Ð573. Devonshire, A. L., nd G. D. Moores A croxylesterse with rod sustrte speciþcity cuses orgnophosphorus, crmte nd pyrethroid resistnce in pech-potto phids (Myzus persice). Pestic. Biochem. Physiol. 18: 235Ð246. Estop, V. F Worldwide importnce of phids s virus vectors. Acdemic, London, United Kingdom. Foster, S. P., I. Deholm, nd A. L. Devonshire The ups nd downs of resistnce in pech-potto phids (Myzus persice) in the UK. Crop Prot. 19: 873Ð 879. Girling, R. D., M. Hssll, J. G. Turner, nd G. M. Poppy Behviorl responses of the phid prsitoid Dieretiell rpe to voltiles from Aridopsis thlin induced y Myzus persice. Entomol. Exp. Appl. 120: 1Ð9. Guerrieri, E., G. Lingu, M. C. Digilio, N. Mss, nd G. Bert Do interctions etween plnt roots nd the rhizosphere ffect prsitoid ehvior? Ecol. Entomol. 29: 753Ð756. Hermn, M.A.B., B. A. Nult, nd C. D. Smrt Effects of plnt growth-promoting rhizocteri on ell pepper production nd green pech phid infesttions in New York. Crop Prot. 27: 996Ð1002. Horsfll, J. L Life history studies of Myzus persice Sulzer. Pennsylvni Agriculturl Experiment Sttion Bulletin 185. Jett, L. W Horticulturl M.U. guide: growing sweet peppers in Missouri. University of Missouri-Columi Extension Service Bulletin G Kloepper, J. W., C. M. Ryu, nd S. Zhng Induced systemic resistnce nd promotion of plnt growth y Bcillus spp. Phytopthology. 94: 1259Ð1266. Kuroli, G., nd Z. S. Lntos Long-term study of lt phid ßight ctivity nd undnce of potto colonizing phid species. Act Phytopthol. Entomol. Hung. 41: 261Ð 273. McGregor, R. R., nd D. R. Gillespie Olfctory responses of the omnivorous generlist predtor Dicyphus hesperus to plnt nd prey odors. Entomol. Exp. Appl : 201. Murphy, J. F., M. S. Reddy, C. M. Ryu, J. W. Kloepper, nd R. Li Rhizocteri-medited growth promotion of tomto leds to protection ginst Cucumer mosic virus. Phytopthology 93: 1301Ð1307. [NASS] Ntionl Agriculturl Sttistics Service New York Stte ell vegetle production. U.S. Deprtment of Agriculture, Wshington, DC. Reiners, S., nd C. H. Petzoldt Integrted crop nd pest mngement guidelines for commercil vegetle production. Cornell Coopertive Extension, Cornell University, Ithc, NY. SAS Institute SAS userõs mnul, version 9.1. SAS Institute, Cry, NC. Thler, J., M. J. Stout, R. Krn, nd S. S. Duffey Jsmonte-medited induced plnt resistnce ffects community of herivores. Ecol. Entomol. 26: 312Ð324. [USDA] U.S. Deprtment of Agriculture United Sttes stndrds for grdes of sweet peppers. U.S. Deprtment of Agriculture, Wshington, DC. University of Cliforni UC IPM pest mngement guidelines: peppers. University of Cliforni Agriculture nd Nturl Resources Puliction vn Loon, L. C., P.A.H.M. Bkker, nd C.M.J. Pieterse Systemic resistnce induced y rhizosphere cteri. Annu. Rev. Phytopthol. 36: 453Ð483. Zehnder, G. W., J. F. Murphy, E. J. Sikor, nd J. W. Kloepper Appliction of rhizocteri for induced resistnce. Eur. J. Plnt Pthol. 107: 39Ð50. Received 22 Septemer 2008; ccepted 2 July 2009.