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1 LETTER doi:1.138/nture11153 Widespred doption of Bt cotton nd insecticide decrese promotes iocontrol services Ynhui Lu 1, Kongming Wu 1, Yuying Jing 2, Yuyun Guo 1 & Nicols Desneux 3 Over the pst 16 yers, vst plntings of trnsgenic crops producing insecticidl proteins from the cterium Bcillus thuringiensis (Bt) hve helped to control severl mjor insect pests 1 5 nd reduce the need for insecticide sprys 1,5,6. Becuse rod-spectrum insecticides kill rthropod nturl enemies tht provide iologicl control of pests, the decrese in use of insecticide sprys ssocited with Bt crops could enhnce iocontrol services However, this hypothesis hs not een tested in terms of long-term lndscpe-level impcts 1. On the sis of dt from 199 to 21 t 36 sites in six provinces of northern Chin, we show here mrked increse in undnce of three types of generlist rthropod predtors (ldyirds, lcewings nd spiders) nd decresed undnce of phid pests ssocited with widespred doption of Bt cotton nd reduced insecticide sprys in this crop. We lso found evidence tht the predtors might provide dditionl iocontrol services spilling over from Bt cotton fields onto neighouring crops (mize, penut nd soyen). Our work extends results from generl studies evluting ecologicl effects of Bt crops 1 4,6,12,13 y demonstrting tht such crops cn promote iocontrol services in griculturl lndscpes. Biologicl control is vlule ecosystem service 14,15, ut incresingly intensive frming strongly influences the popultions of nturl enemies nd the iocontrol services they provide However,lndscpeiodiversity mngement nd restricted use of pesticides my enhnce iocontrol services in gro-ecosystems nd could thus fvour the development of sustinle frming 7 9. Geneticlly engineered crops tht express d-endotoxins (Cry proteins) from Bcillus thuringiensis (Bt) hve een incresingly implemented y frmers in mny countries since 1996, nd more thn h of Bt crops were plnted worldwide in 211 (ref. 19). Bt crops hve successfully controlled severl mjor insect pests 1,2,4,5 nd led to drstic decrese in insecticide use on these crops 1,5,6. Becuse insecticide pplictions hve een grdully reduced in Bt crops, their widespred doption my enefit nturl enemies nd my therefore potentilly enhnce ssocited ecosystem services such s the control of rthropod pests This lst point hs not yet een documented, especilly with regrd to the long-term lndscpe-level impcts 1. From the 197s, insecticides were pplied extensively to control cotton ollworm (CBW), Helicoverp rmiger, the most serious insect pest on conventionl cotton in Chin. However, control ecme lmost impossile in the erly 199s ecuse the pest ecme resistnt to most insecticides, nd unprecedented outreks in 1992 led to wide overuse of insecticides. Consequently, in 1993, the Chinese government requested systemtic insecticide pplictions in whet crops for the control of the first-genertion CBW; tht is, efore the following genertions colonized cotton crops 2. Although insecticide use decresed in cotton, this mesure ws not sustinle ecuse insecticide pplictions were incresed on whet crops, resulting in oth higher costs nd environmentl pollution. Bt cotton ws therefore pproved in 1997 for commercil use to control CBW, nd it ecme the Chinese government s key mesure ginst this cotton pest. It ws rpidly plnted on lrge scle, rising to h y 211 (more thn 95% of the cotton crop in northern Chin). It mnged CBW effectively, which led to decresed insecticide use on this pest 3,21. The widespred doption of Bt cotton my hve fvoured n increse in generlist nturl enemy popultions nd promoted their ssocited iocontrol services. We therefore performed two ssessments: first, whether implementing Bt cotton on lrge scle induced n increse in popultions of three groups of key generlist predtors in Chin (ldyirds, lcewings nd spiders) in oth Bt cotton nd three common neighouring crops, nmely mize, penut nd soyen; nd second, whether this trend resulted in incresed iocontrol services in griculturl lndscpes in Chin. Aphids were selected s pest model ecuse they re common prey for generlist predtors. During , reserch ws conducted in six mjor cotton-growing provinces (Henn, Heei, Shndong, Shnxi, Anhui nd Jingsu) in northern Chin, where out h of cotton nd h of other crops (notly mize, penut nd soyen) re cultivted nnully y more thn ten million smll-scle frmers. Predtors per 1 plnts Aphids per 1 plnts ( 1 3 ) Yer Figure 1 Popultion densities of predtors nd phids on cotton with different mngement regimes t Lngfng experimentl sttion (21 211)., Predtors., Aphids. The lue nd red lines indicte Bt cotton nd non-bt cotton without insecticide sprys, respectively; the green line represents non-bt cotton with CBW insecticide sprys (chemicl control) Stte Key Lortory for Biology of Plnt Diseses nd Insect Pests, Institute of Plnt Protection, Chinese Acdemy of Agriculturl Sciences, Beijing, 1193 Chin. 2 Ntionl Agro-Technicl Extension nd Service Center, Beijing, 126 Chin. 3 French Ntionl Institute for Agriculturl Reserch (INRA), UMR1355-ISA, 4 route des chppes, 693 Sophi-Antipolis, Frnce. 212 Mcmilln Pulishers Limited. All rights reserved MONTH 212 VOL NATURE 1

2 RESEARCH LETTER Predtors nd cotton phids were smpled from 21 to 211 in Bt nd non-bt cotton plots t Lngfng experimentl sttion in Heei province. No significnt differences were found for predtor (P 5.341) nd phid (P 5.555) undnces etween Bt cotton nd non-bt cotton with similr mngement methods; tht is, without ppliction of insecticide (Fig. 1, nd Supplementry Tle 1, ). However, predtor undnce ws significntly lower nd phid undnce ws significntly higher in plots treted with insecticides for CBW mngement in comprison with insecticide-free plots (P,.1) (Fig. 1, nd Supplementry Tle 1, ), lthough it vried over yers (significnt interctions etween insecticide ppliction nd yer). Bt cotton does not itself ffect predtor nd phid popultion levels 1,22, nd generlist predtors re clerly susceptile to rod-spectrum insecticides (such s synthetic pyrethroids) used ginst CBW. Therefter, insecticide-induced phid resurgence usully occurs with widespred pplictions of insecticides. Predtor undnce nd insecticide use in cotton were monitored in 36 loctions throughout northern Chin during (Fig. 2 nd Supplementry Tle 2). Predtor popultion levels grdully incresed over tht period, nd reltively high popultion levels were lwys oserved fter Bt cotton ws implemented in 1997 (Fig. 2). In 14 selected loctions, ll three mjor groups of predtors (ldyirds, lcewings nd spiders) showed n incresing trend similr to tht of the whole predtor complex (Fig. 2). Insecticide use ptterns lso chnged gretly with Bt cotton implementtion. After the introduction of Bt cotton, the numer of insecticide sprys ginst CBW (nd other insect pests in generl), minly pyrethroid nd orgnophosphte insecticides (Supplementry Tle 3), which hve multiple negtive effects on nturl enemies 17, ws lower thn during the pre-bt cotton period, nmely (Fig. 2c). Moreover, predtor popultion level nd numer of insecticide sprys were positively nd negtively relted to Bt cotton plnting proportions, respectively (P,.1; Supplementry Fig. 1, ), nd indicted the effect of its lrge-scle doption on the predtor popultion trend. Regression nlyses showed tht fewer insecticide sprys ginst CBW nd ll insect pests were correlted to gret extent with n increse in predtor popultions in northern Chin (P,.1) (Fig. 2d, e). The results were consistent in the six provinces, nd insecticide use ginst CBW ws driving fctor for predtor popultion level in the cotton groecosystem (ll P,.5; Supplementry Tle 4). Cotton phid undnce ws surveyed in 24 loctions from 199 to 21 (Supplementry Tle 2) to ssess the iocontrol services provided y generlist predtors. Liner regression nlyses showed tht incresing generlist predtor popultions were correlted with decresing phid undnce in northern Chin in generl (P,.1; Fig. 3) nd in ll provinces except Shnxi (Supplementry Fig. 2 e). During the three min periods studied tht is, without Bt cotton, with less thn 9% nd more thn 9% of Bt cotton plnting in the lndscpes phid popultions decresed significntly (P,.1; Fig. 3). In ddition, phid popultion ws negtively relted to the proportion of Bt cotton plnted (P 5.3; Supplementry Fig. 3). Exclusion cge trils in 21 nd 211 t Lngfng nd Xinxing experimentl sttions (in 4 N 35 N 3 N Heei Shnxi Shndong Henn Jingsu N Anhui W E S km 11 E 115 E 12 E 125 E Predtors per 1 plnts c Sprys per seson d Predtors per 1 plnts e Insecticide sprys per seson Figure 2 Reltionships etween predtor popultion density nd numer of insecticide sprys on cotton in northern Chin (199 21)., Survey loctions, indicted y red dots., Predtor popultion density on cotton in commercil fields in 36 loctions (ech point represents one-yer dt; the red rrow indictes the eginning of Bt cotton use). Inset: popultion undnce of ldyirds (lue), spiders (red) nd lcewings (green), collected from 14 loctions. c, Numer of insecticide sprys for CBW (grey points) nd ll insect pests (lck points) on cotton; ech point represents one-yer dt. d, Liner reltionship etween totl numer of insecticide pplictions, determined y pooling ll tretments ginst ll the insect pests on cotton (x), nd the predtor undnce (y) in cotton (y x , F 1, , R , P,.1). e, Liner reltionship etween numer of insecticide pplictions for CBW only (x) nd predtor undnce (y) (y x , F 1, , R , P,.1). The dt in d nd e re replotted from nd c. All error rs show s.e.m. Predtors per 1 plnts CBW insecticide sprys per seson 2 NATURE VOL MONTH Mcmilln Pulishers Limited. All rights reserved

3 LETTER RESEARCH Aphids per 1 plnts Aphids per 1 plnts 6, 5, 4, 3, 2, 1, Predtors per 1 plnts Predtors per 1 plnts 6, 5, 4, 3, 2, 1, Yer Figure 3 Popultion undnce of cotton phid in northern Chin (199 21) nd reltionship with predtor undnce on cotton., Regression nlysis etween undnce of phids (y) (log e -trnsformed) nd predtor undnce (x) (y 5 e 2.15x , F 1, , R , P,.1)., Aphid popultion density on cotton in commercil fields in 24 loctions (ech point represents one-yer dt, nd the red rrow indictes the eginning of Bt cotton use). Red lines show the men popultion density of phids in cotton fields during three min periods, nmely efore Bt cotton plnting ( ), when Bt cotton plnting ws less thn 9% of cotton surfces plnted ( ) nd when it ws more thn 9% (24 21). Red lines ering different letters re significntly different t the P,.5 level in lestsignificnt-difference post-hoc tests (one-wy nlysis of vrince on log e - trnsformed dt: F 2, , P,.1). All error rs show s.e.m. Heei nd Henn provinces, respectively) further demonstrted the significnt effects of predtors on phid popultion growth in cotton fields (Supplementry Fig. 4, ). As the cotton phid popultions declined, n invsive whitefly in cotton, Bemisi tci 2, proly served s n lterntive prey for the incresing predtor popultions. c All these results indicte tht the widespred doption of Bt cotton ultimtely promotes iocontrol services in the groecosystem ecuse decresed insecticide use leds to n increse in predtor popultions. Brodly speking, mesures tht preserve predtors in cotton fields gretly help to control phid popultions; for exmple, when insecticide pplictions in whet were requested y the Chinese government ( ) to prevent CBW outreks in cotton (see ove), it led to decresing trend in phid undnce (Fig. 3). Predtor undnce ws lso monitored from 21 to 211 in three neighouring crops: mize, penut nd soyen t Lngfng experimentl sttion. There ws positive reltionship etween predtor undnce in cotton nd soyen (P 5.19; Fig. 4), s well s etween cotton nd penut (mrginlly significnt, P 5.75; Fig. 4). We oserved similr trend in mize ut it ws not significnt (P 5.216; Fig. 4c). The incresed predtor undnce in mize ws linked to decrese in phid pest undnce in tht prticulr crop (mrginlly significnt, P 5.61; Fig. 4d). Biocontrol services re importnt components in gro-ecosystems nd could led to the development of sustinle griculture 7,15,23.In conventionl griculturl prctices, insecticides re frequently used to control trgeted pests, ut they cn led to outreks of secondry pests y suppressing their nturl enemies 24. This so-clled insecticideinduced resurgence ws first reported for cotton phid in the 197s nd ws regrded s key fctor leding to popultion outreks of this pest in Chin 25. Our work demonstrtes the importnce of nturl enemies in the long-term suppression of the cotton phid. The widespred doption of Bt cotton, s sustinle mesure to reduce insecticide use, hs indirectly promoted generlist predtor undnce in Bt cotton fields ut lso to smller extent in three common djcent crops in northern Chin. Bt crops therefore might enhnce iocontrol services in griculturl lndscpes through n incresed undnce of generlist nturl enemies. This study provides key informtion on long-term lndscpe-level ecologicl effects of Bt crops s well s useful insights, for exmple into the mngement of pest resurgence prolems reported for mny pests worldwide 26. Generlist predtors usully hve gret dispersl ility nd cn rely on vrious food sources. Hence, not only cn they synchronously ttck different insect pests in one field, ut they cn lso colonize different hitts in different sesons 27,28. Furthermore, some hitt mngement mesures, such s inter-plnting different crops or wild plnts, hve een dopted to provide resources such s food supply or shelter for nturl enemies, thus incresing conservtion iologicl control in djcent fields 7,9,27,28. We hve demonstrted tht decresing insecticide ppliction, through widespred Bt cotton plntings, sustined generlist predtors nd helped to suppress phid popultions in this Predtors per 1 plnts (soyen) c Predtors per 1 plnts (mize) Predtors per 1 plnts (cotton) 4 Predtors (cotton) per 1 plnts (cotton) d Predtors per 1 plnts (cotton) Predtors per 1 plnts (penut) Aphids per 1 plnts (mize) Predtors per 1 plnts (cotton) Predtors per 1 plnts (cotton) 2,5 (cotton) 2, 1,5 1, Predtors per per 1 1 plnts plnts (mize) Figure 4 Reltionships etween predtor undnce on cotton nd in three other crops, nd etween predtor nd phid undnces in mize. Dt on soyen (21 211), penut (21 25 nd ) nd mize (21 23 nd ) were collected t Lngfng experimentl sttion., Liner reltionship etween predtor undnce on cotton (x) nd on soyen (y) (y 5.1x , F 1, , R , P 5.191)., Liner reltionship etween predtor undnce on cotton (x) nd on penut (y) (y 5.9x , F 1, , R , P 5.747). c, Liner reltionship etween predtor undnce on cotton (x) nd on mize (y) (y 5.23x , F 1,5 5 2., R , P ). d, Reltionship etween predtor undnce (x) nd undnce of phids in mize (y; log e -trnsformed dt) (y 5 e 2.7x , F 1, , R , P 5.61). All error rs show s.e.m. 212 Mcmilln Pulishers Limited. All rights reserved MONTH 212 VOL NATURE 3

4 RESEARCH LETTER crop. Lrge-scle insecticide reduction is the key driver in such processes (for exmple see the period , during which insecticide decrese fvoured n increse in predtor popultions nd decline of phid popultions). Higher generlist predtor popultion levels in Bt cotton led to lower insect pest levels in the crop, nd these predtors might provide dditionl iocontrol services spilling over from cotton fields onto neighouring crops, lthough further work should e performed to document this lst point. Brodly speking, the deployment of Bt crops my fvour iocontrol services nd enhnce economic enefits not only in Bt crop fields ut lso in the whole griculturl lndscpe. Field studies indicted tht Bt crops protected nturl enemies in comprison with non-bt crops, which rely on conventionl insecticides 22,29. Our present study, demonstrting tht iocontrol services re potentilly provided y Bt crops throughout the griculturl lndscpe, my offer new options in developing conservtion iologicl control mesures t the lndscpe level. Criticl concerns out the ecologicl risk ssessment of trnsgenic crops still remin, especilly on lrge scle 29. The present study confirms no negtive effects of one Bt crop, Bt cotton, on generlist predtors in griculturl lndscpes in Chin. More prticulrly, we hve demonstrted mrked increse in generlist predtor popultion levels nd ssocited iocontrol services linked to decresed insecticide use owing to the widespred doption of the Bt crop. Our work provides comprehensive, long-term nd lrge-scle ssessment of the possile ecologicl nd griculturl effects of trnsgenic crops. METHODS SUMMARY The study ws sed on lrge-scle surveys of predtor nd cotton phid popultions in cotton fields of northern Chin from 199 to 21 nd on experiments nd surveys tht were performed t Lngfng experimentl sttion of the Chinese Acdemy of Agriculturl Science (CAAS) during the period The surveys nd experiments focused on three mjor generlist predtor groups (ldyirds, lcewings nd spiders) nd on phid pests in cotton nd in three common cotton-neighouring crops, nmely mize, penut nd soyen. At the CAAS, we first ssessed how culturl prctices could ffect predtor nd phid popultions in the long term in cotton fields; cotton plots were estlished every yer nd the undnce of predtors nd cotton phids ws surveyed in three different plot types: Bt cotton, non-bt cotton nd non-bt cotton with insecticide. Second, we determined the impct of predtors on phid popultion in cotton y mens of exclusion cge trils. Third, we evluted the impct of implementing Bt cotton on predtor nd phid popultions in the neighouring crops. Field plots were estlished in cotton, mize, penut nd soyen, nd popultion dynmics of predtors nd phids were monitored. Lrge-scle surveys were conducted in six provinces in northern Chin (36 loctions, 1 2 fields per loction) to evlute the impct of insecticide pplictions on the undnce of predtors nd phids in cotton fields. We tested, first, the reltionship etween predtor undnce nd insecticide use during the period (tht is, including the period efore nd during the widespred doption of Bt cotton y frmers), nd second, how cotton phid density ws relted to predtor undnce during the sme period. Full Methods nd ny ssocited references re ville in the online version of the pper t Received 3 Jnury; ccepted 23 April 212. Pulished online 13 June Shelton, A. M., Zho, J. Z. & Roush, R. T. Economic, ecologicl, food sfety, nd socil consequences of the deployment of Bt trnsgenic plnts. Annu. Rev. Entomol. 47, (22). 2. Crriere, Y. et l. Long-term regionl suppression of pink ollworm y Bcillus thuringiensis cotton. Proc. Ntl Acd. Sci. USA 1, (26). 3. Wu, K. M., Lu, Y. H., Feng, H. Q., Jing, Y. Y. & Zho, J. Z. Suppression of cotton ollworm in multiple crops in Chin in res with Bt toxin-contining cotton. Science 321, (28). 4. Hutchison, W. D. et l. Arewide suppression of Europen corn orer with Bt mize reps svings to non-bt mize growers. Science 33, (21). 5. Tshnik, B. E. et l. Suppressing resistnce to Bt cotton with sterile insect releses. Nture Biotechnol. 28, (21). 6. Cttneo, M. G. et l. Frm-scle evlution of the impcts of trnsgenic cotton on iodiversity, pesticide use, nd yield. Proc. Ntl Acd. Sci. USA 13, (26). 7. Lndis, D. A., Wrtten, S. D. & Gurr, G. M. Hitt mngement to conserve nturl enemies of rthropod pests in griculture. Annu. Rev. Entomol. 45, (2). 8. Crowder, D. W., Northfield, T. D., Strnd, M. R. & Snyder, W. E. Orgnic griculture promotes evenness nd nturl pest control. Nture 466, (21). 9. Winqvist, C. et l. Mixed effects of orgnic frming nd lndscpe complexity on frmlnd iodiversity nd iologicl control potentil cross Europe. J. Appl. Ecol. 48, (211). 1. Romeis, J. et l. Trnsgenic crops expressing Bcillus thuringiensis toxins nd iologicl control. Nture Biotechnol. 24, (26). 11. Ble, J. S., vn Lenteren, J. C. & Bigler, F. Biologicl control nd sustinle food production. Phil. Trns. R. Soc. B 363, (28). 12. Gtehouse, A. M. R., Ferry, N., Edwrds, M. G. & Bell, H. A. Insect-resistnt iotech crops nd their impcts on eneficil rthropods. Phil. Trns. R. Soc. B 366, (211). 13. Wolfenrger, L. L., Nrnjo, S. E., Lundgren, J. G., Bitzer, R. J. & Wtrud, L. S. Bt crop effectsonfunctionlguildsofnon-trget rthropods: met-nlysis. PLoSONE 3, e /journl.pone.2118 (28). 14. Binchi, F. J. J. A., Booij, C. J. H. & Tschrntke, T. Sustinle pest regultion in griculturl lndscpes: review on lndscpe composition, iodiversity, nd nturl pest control. Proc. R. Soc. Lond. B 273, (26). 15. Losey, J. E. & Vughn, M. The economic vlue of ecologicl services provided y insects. Bioscience 56, (26). 16. Chpin, F. S. et l. Consequences of chnging iodiversity. Nture 45, (2). 17. Desneux, N., Decourtye, A. & Delpuech, J. M. The sulethl effecs of pesticides on eneficil rthropods. Annu. Rev. Entomol. 52, (27). 18. Lndis, D. A., Grdiner, M. M., vn der Werf, W. & Swinton, S. M. Incresing corn for iofuel production reduces iocontrol services in griculturl lndscpes. Proc. Ntl Acd. Sci. USA 15, (28). 19. Jmes, C. Glol Sttus of Commercilized Biotech/GM crops: 211 (ISAAA rief no. 43, Interntionl Service for the Acquisition of Agri-Biotech Applictions, 211). 2. Wu, K. M. & Guo, Y. Y. The evolution of cotton pest mngement prctices in Chin. Annu. Rev. Entomol. 5, (25). 21. Lu, Y. H. et l. Mirid ug outreks in multiple crops correlted with wide-scle doption of Bt cotton in Chin. Science 328, (21). 22. Nrnjo, S. E. Long-term ssessment of the effects of trnsgenic Bt cotton on the undnce of nontrget rthropod nturl enemies. Environ. Entomol. 34, (25). 23. Rgsdle, D. W., Lndis, D. A., Brodeur, J., Heimpel, G. E. & Desneux, N. Ecology nd mngement of the soyen phid in North Americ. Annu. Rev. Entomol. 56, (211). 24. Hrdin, M. R. et l. Arthropod pest resurgence: n overview of potentil mechnisms. Crop Prot. 14, 3 18 (1995). 25. Wu, K. W. & Liu, Q. X. Study on the resurgence cused y insecticides for cotton phid, Aphis gossypii. Act Ecol. Sin. 12, (1992). 26. Ro, C. N., Shivnkr, V. J. & Singh, S. in Encyclopedi of Pest Mngement Vol 2 (ed. Pimentel, D.) (CRC Press, 27). 27. Symondson, W. O. C., Sunderlnd, K. D. & Greenstone, H. M. Cn generlist predtors e effective iocontrol gents? Annu. Rev. Entomol. 47, (22). 28. Tschrntke, T. et l. Conservtion iologicl control nd enemy diversity on lndscpe scle. Biol. Control 43, (27). 29. Romeis, J., Shelton, A. M. & Kennedy, G. G. Integrtion of Insect-resistnt Geneticlly Modified Crops within IPM Progrms (Springer, 28). Supplementry Informtion is linked to the online version of the pper t Acknowledgements Wethnk thegriculturl technicinsofthe 36 surveyedloctions for providing dt sets from cotton fields; W. Li nd L. Wng for providing the predtor exclusion cge dt sets; Y. Zhng nd C. Li for ssistnce in mking the survey mp; H. Yun for help in prepring the list of insecticides in cotton; ndr. Senoussi for dvice on dt nlyses. This work ws funded y the Key Project for Breeding Geneticlly Modified Orgnisms (grnt no. 211ZX812-4) nd the Interntionl Science nd Technology Coopertion Project (grnt no. 21DFA322). Author Contriutions K.W., Y.L. nd Y.G. designed nd performed the experiments. Y.J. performed the surveys. Y.L., K.W. nd N.D. nlysed the dt nd shred in the scoping nd writing responsiilities. Author Informtion Reprints nd permissions informtion is ville t The uthors declre no competing finncil interests. Reders re welcome to comment on the online version of this rticle t Correspondence nd requests for mterils should e ddressed to K.W. (kmwu@ippcs.cn). 4 NATURE VOL MONTH Mcmilln Pulishers Limited. All rights reserved

5 LETTER RESEARCH METHODS Aphid pests nd predtor complex considered in the study. In northern Chin, severl phid species re reported s pests on cotton, mize, penut nd soyen. Aphis gossypii Glover (cotton phid) is the min phid pest in cotton fields in northern Chin where there re two key iotypes (clled seedling nd summer phids, respectively). Only the summer phid, which colonizes fields from erly July to lte August, is considered mjor cotton pest 2,3,31. The seedling phid is controlled y insecticide tretments pplied on the seeds; these compounds do not lst long enough within plnts to provide control of the summer phid 2. Rhoplosiphum midis Fitch, R. pdi Linneus nd Sitoion vene Fricius re the three dominnt phid pest species on mize 31, nd A. glycines Mtsumur nd A. crccivor Koch re the min phid species on soyen nd penut, respectively 31. In our study, the ove phid species were considered in ssessing the iocontrol services provided y generlist predtors. In northern Chin, there re three dominnt groups of generlist predtors in cotton field (more thn 9% of ll the predtors 3 ): ldyirds, lcewings nd spiders. In our study we therefore focused on predtor complex composed of ldyirds (Propyle jponic Thunerg, Hrmoni xyridis Plls, Coccinell septempunctt L. nd Adoni vriegt Goeze), lcewings (Chrysop septempunctt Wesmel, Chrysoperl sinic Tjeder nd Chrysop formos Bruer) nd spiders (Erigonidium grminicolum Sundevll, Misumenopos tricuspidt Fhricius nd Prdos t-insignit Boes. et Str.); these compose the most common predtors in griculturl lndscpe of tht region. These groups of predtors re lso common in mize, penut nd soyen fields nd were thus lso considered s predtor complex for these three crops Impct of griculturl prctices on predtor nd cotton phid popultions. Survey experiments were conducted from 21 to 211 t Lngfng experimentl sttion (39.53u N, 116.7u E), Chinese Acdemy of Agriculturl Sciences (CAAS), Heei province, Chin. Fifteen cotton plots (4 m 2 ech) were estlished every yer nd were mnged with gronomic prctices tht re stndrd in northern Chin. A rndomized lock design with three replictes ws used, which included two Bt nd two conventionl cotton vrieties. One Bt cotton vriety expressing Cry1Ac (NuCOTN33B) nd nother Bt cotton vrieties expressing Cry1A (SGK321) were supplied y Monsnto Co. nd the Biotechnology Reserch Institute, CAAS, respectively. Two conventionl cotton vrieties (Shiyun321 nd Zhong12) were otined from the Institute of Plnt Protection, CAAS. Shiyun321 ws the non-trnsgenic isoline of SGK321. Every yer, the tril consisted of three tretments: Bt cotton nd non-bt cotton plots without insecticide, nd non-bt cotton (one vriety, Zhong12) plots with insecticides. -Cypermethrin (pyrethroid) nd phoxim (orgnophosphte) were used when insecticides were pplied. The choice of these two insecticides, nd their frequency of ppliction, were oth sed on mngement guidelines for CBW (Helicoverp rmiger) used throughout the erly 199s in northern Chin 2 (Supplementry Tle 3). The undnces of predtors nd cotton phid were surveyed in the three cotton plot types (Bt cotton, non-bt cotton nd non-bt cotton with insecticide) every 4 or 5 dys from mid-june to lte August from 21 to 211. At ech smpling dte, 1 plnts t five rndom loctions per plot 35 were visully inspected nd ll predtors nd phids were recorded. No significnt differences (P..5) were found etween cotton vrieties, so we comined NuCOTN33B nd SGK321 s Bt cotton, nd Shiyun321 nd Zhong12 s non-bt cotton, for further nlysis. A three-wy ANOVA ws used to nlyse the effects of the cotton vriety (Bt cotton nd non-bt cotton), insecticide tretments (chemicl control nd non-chemicl control) nd smpling yer on predtor nd phid undnce, nd the interctions etween yer nd cotton vriety, nd etween yer nd insecticide spry; the mens were compred y the lest-significnt-difference (LSD) test t P 5.5. Survey of predtors nd cotton phid in cotton crops in northern Chin. From 199 until 21, commercil cotton fields in 36 loctions in six provinces (Henn, Heei, Shndong, Shnxi, Anhui nd Jingsu) of northern Chin were surveyed for predtors nd cotton phid (Supplementry Tle 2). Insect popultions were recorded every 3 1 dys from erly June to lte August every yer. For ech survey, 1 2 cotton fields were smpled per loction. Within ech field, totl of 5 1 cotton plnts t five rndom loctions were visully inspected for predtors 3. Among the 36 loctions, ldyirds, lcewings nd spiders were recorded s predtor complex in 22 loctions, wheres in 14 sites the three predtor types were recorded individully. The 14 loctions included Anxin nd Xinji from Heei province; Dezhou, Binzhou nd Chengwu from Shndong province; Ruicheng, Yongji nd Linfen from Shnxi province; Dongzhi, Wngjing nd Tihu from Anhui province; nd Dfeng, Tongzhou nd Himen from Jingsu province. The cotton phid popultions were surveyed in 24 loctions in five provinces (Supplementry Tle 2), using the sme smpling schedule s for survey of predtors 3. On ech plnt, n upper lef, middle lef nd lower lef were exmined for phid presence. At the sme time, ll insecticide pplictions (for mngement of CBW nd other rthropod pests) were recorded per field per yer. Liner regression nlyses were used to ssess the reltionship etween predtor undnce nd insecticide use on the dt set gthered from 199 to 21 tht is, including the period during which Bt cotton ws incresingly dopted in Chin y frmers. Both simple nd forwrd stepwise regressions were used to relte predtor undnce nd insecticide use ginst CBW nd ll insect pests for ech province nd the whole of northern Chin in the dt set. Simple liner models were used to ssess the reltionship etween phid density (log-trnsformed) nd predtor undnce from erly July to lte August (in the dt set) for ech province nd for the whole of northern Chin. Liner regression nlyses were used to ssess the reltionship etween predtor undnce nd phid undnce (log-trnsformed) with Bt cotton plnting proportions. In this nlysis, the men undnces of predtors nd phids during were included s the dt when the Bt cotton plnting proportion ws. To evlute the impct of the predtors on cotton phid popultion further, exclusion cge trils were conducted in 21 nd 211 t Lngfng experimentl sttion nd Xinxing experimentl sttion of CAAS (Henn Province, 35.9u N, u E). This tril included cged tretment nd n open-field tretment s control 18,36. The cge ws 2 m wide y 2 m wide y 1.5 m high nd mde from the insect mesh net, which llowed the emigrtion nd immigrtion of lte phids nd its prsitoids, ut locked the predtors 37. Ten cotton plnts were covered in ech cge. This tril egn in July, when lmost only pterous phids were in the field 38, nd ws limited to 15 dys to prevent the ppernce of lte phids in the cge 18,36. At ech site, cge tretments with three or four replictes were estlished when phid density reched n verge of 2 individuls per plnt in 21 nd 2 individuls per plnt in 211. We recorded the phid undnce 15 dys fter tretment. Menwhile, predtor densities were surveyed three times, on dy, dy 5 nd dy 1, in ten rndomly selected cotton plnts in open field during the whole tril. The phid undnce in cged nd open plnts ws compred y one-wy ANOVA followed y post-hoc LSD test. Before nlysis, the dt for phid undnce were log e -trnsformed. Impct of Bt cotton doption on popultions of predtors in neighouring crops. Popultion dynmics of the predtor complex were monitored in cotton, soyen, penut nd mize field plots from 21 to 211 (except for mize, which ws monitored during nd , nd soyen, which ws monitored during nd ) t Lngfng experimentl sttion. Every yer, totl of nine field plots (4 m 2 ech) were estlished for ech crop type nd they were mnged in the sme wy, pplying the sme fertilizers nd irrigtion tretment, free of ny pesticide. A rndomized lock design with three replictes for ech crop type ws used. One Bt cotton vriety, SGK321, ws supplied y the Biotechnology Reserch Institute (CAAS); the mize (vr. Shengshi29), soyen (vr. Zhonghung13) nd penut (vr. Huyu16) were provided y Lngfng experimentl sttion (CAAS), the Institute of Crop Sciences (CAAS) nd the Shndong Penut Reserch Institute, respectively. The undnce of predtors ws recorded in the four different crops (Bt cotton, mize, penut nd soyen) every four or five dys from mid-june to lte August. At ech smpling dte, 1 plnts in five rndom spots per plot were visully inspected nd ll predtors were recorded. Liner regression nlyses were used to ssess the reltionship etween sesonl density of predtors on cotton nd soyen/penut (dt set covering the period) nd mize (dt set covering the nd periods). For the mize plots, mize phids were lso recorded ecuse they re well known s the min pests on mize in northern Chin. Popultion levels of phids on soyen nd penut crops t Lngfng experimentl sttion were very low during the course of our study nd therefore the dt could not e considered in the frmework of the study. A simple liner model ws used to ssess the reltionship etween phid undnce (log-trnsformed) nd predtor undnce on mize. 3. Qu, X. F. Cotton Pest Forecst in Chin: the Criterion, Zoning nd Method (Chin Scien-tech Press, 1992). 31. Institute of Plnt Protection, Chinese Acdemy of Agriculturl Sciences. Crop Diseses nd Pests in Chin (Chin Agriculturl Press, 1995). 32. Xu, H. F., Mu, S. M., Xu, Y. Y., Mu, J. Y. & Dong, C. X. On the community structure of mjor insect pests nd nturl enemies in summer corn field inlid in cotton re. Act Phytophyl. Sin. 27, (2). 33. Yng, Q. M., Sun, M., Xu, Y. F., Shi, A. J. & Mu, J. Y. On the community structure of mjor insect pests nd nturl enemies in summer en field. J. Shndong Agric. Univ. 35, (24). 34. Ding, Y. Q. & Cheng, S. L. Preliminry investigtion nd utiliztion of nturl enemies of phid in penut field. J. Penut Sci. 39, (21). 212 Mcmilln Pulishers Limited. All rights reserved

6 RESEARCH LETTER 35. Wu, K. M. & Guo, Y. Y. Influences of Bcillus thuringiensis Berliner cotton plnting on popultion dynmics of the cotton phid, Aphis gossypii Glover, in northern Chin. Environ. Entomol. 32, (23). 36. Grdiner, M. M. et l. Lndscpe diversity enhnces iologicl control of n introduced crop pest in the north-centrl USA. Ecol. Appl. 19, (29). 37. Mio, J., Wu, K. M., Hopper, K. R. & Li, G. X. Popultion dynmics of Aphis glycines (Homopter: Aphidide) nd impct of nturl enemies in northern Chin. Environ. Entomol. 36, (27). 38. Lu, Y. H., Qi, F. J. & Zhng, Y. J. Integrted Mngement of Diseses nd Insect Pests in Cotton (Golden Shield Press, 21). 212 Mcmilln Pulishers Limited. All rights reserved