SELECTIVITY OF INSECTICIDES USED IN PEACH FARMING TO LARVAE OF. Chrysoperla externa (NEUROPTERA: CHRYSOPIDAE) EM SEMICAMPO CONDITIONS 1

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1 Universidde Federl Rurl do Semi-Árido Pró-Reitori de Pesquis e Pós-Grdução ISSN X (impresso) ISSN (online) SELECTIVITY OF INSECTICIDES USED IN PEACH FARMING TO LARVAE OF Chrysoperl extern (NEUROPTERA: CHRYSOPIDAE) IN SEMI-FIELD CONDITIONS 1 RODOLFO VARGAS CASTILHOS 2 *, ANDERSON DIONEI GRÜTZMACHER 3, MÁRCIO BARTZ DAS NEVES 3, ÍTALO LUCAS DE MORAES 3, CLEITON JAIR GAUER 3 ABSTRACT The selectivity of five insecticides, regulrly used in pech frming, ws ssessed for lrve of the predtor Chrysoperl extern (Hgen) (Neuropter: Chrysopide) by mens of biossy in semi-field conditions. The biossy ws bsed on the counting of cptured lrve fter relese in pech trees treted with the insecticides (% of ctive ingredient in spry liquid): deltmethrin (0.001), fenthion (0.050), phosmet (0.100), lufenuron (0.005) nd mlthion (0.200). Bit-crds with eggs of Angst kuehniell (Zeller) (Lepidopter: Pyrlide) were used to cpture lrve from treted plnts; five of them were fixed in plnt cnopy nd five others left on the soil round stem. A protective brrier mde up of glvnized steel sheet ws used for ech plnt to void loss of lrve. The number of lrve feeding on the bit-crds ws mesured for four dys. According to the number of cptured lrve, ech insecticide effect ws estimted nd clssified into toxicity ctegories s stted by the Interntionl Orgniztion for Biologicl nd Integrted Control of Noxious Animls nd Plnts (IOBC). Bsed on observtions, the insect growth regultor lufenuron ws hrmless, while the neurotoxins deltmethrin nd mlthion were slightly hrmful; nd lstly, fenthion nd phosmet were modertely hrmful to C. extern lrve in semi-field conditions. Thus, lufenuron should be recommended for integrted pest mngement, since it would preserve this predtor species in pech orchrds. Key words: Biologicl control. Lcewings. Chemicl control. Prunus persic L.. SELETIVIDADE DE INSETICIDAS EMPREGADOS NA PERSICULTURA PARA LARVAS DE Chrysoperl extern (NEUROPTERA: CHRYSOPIDAE) EM SEMICAMPO RESUMO A seletividde de cinco inseticids utilizdos em pomres de pessegueiro foi vlid sobre lrvs do preddor Chrysoperl extern (Hgen) (Neuropter: Chrysopide) por meio de bioensio conduzido em semicmpo. O bioensio bseou-se n contgem do número de lrvs cpturds pós liberção em plnts de pessegueiro trtds com os inseticids (% de ingrediente tivo n cld) deltmetrin (0,001), fention (0,050), fosmete (0,100), lufenurom (0,005) e mltion (0,200). Pr cptur ds lrvs ns plnts trtds form utilizdos dez crtões-isc contendo ovos de Angst kuehniell (Zeller) (Lepidopter: Pyrlide), sendo cinco fixdos n cop e cinco fixdos no solo o redor do cule. Um brreir de proteção compost por chp de ço glvnizdo foi utilizd em cd plnt pr evitr perd de lrvs. O número de lrvs limentndo-se nos crtões foi mensurdo durnte qutro dis. Em função do número de lrvs cpturds, o efeito de cd inseticid foi clculdo e clssificdo ns ctegoris de toxicidde segundo Interntionl Orgniztion for Biologicl nd Integrted Control of Noxious Animls nd Plnts (IOBC). Bsedo no efeito observdo, o reguldor de crescimento lufenurom foi inofensivo, enqunto os neurotóxicos deltmetrin e mltion form pouco tóxicos, e fention e fosmete form moderdmente tóxicos lrvs de C. extern em condições de semicmpo. Dest form, lufenurom deve ser recomenddo no mnejo integrdo de prgs fim de se preservr est espécie de preddor em pomres de pessegueiro. Plvrs-chve: Controle biológico. Crisopídeo. Controle químico. Prunus persic L.. *Corresponding uthor 1 Received for publiction in 07/08/2015; ccepted in 06/16/2016. Pper extrcted from the doctorl thesis of the first uthor, Funded by CAPES, CNPq nd FAPERGS. 2 Reserch Center for Fmily Frming, Empres de Pesquis Agropecuári e Extensão Rurl de Snt Ctrin, Chpecó, SC, Brzil; rodolfocstilhos@epgri.sc.gov.br. 3 Deprtment of Crop Protection, Universidde Federl de Pelots, Pelots, RS, Brzil; dgrutzm@ufpel.edu.br, mbdsneves@hotmil.com, itlolucsmores@gmil.com, cleitonjguer@gmil.com. Rev. Cting, Mossoró, v. 30, n. 1, p , jn. mr.,

2 SELECTIVITY OF INSECTICIDES USED IN PEACH FARMING TO LARVAE OF Chrysoperl extern (NEUROPTERA: R. V. CASTILHOS et l. INTRODUCTION Among the dmging fctors in pech yields in Brzil, it is noteworthy mention the infesttions of pest-insects such s fruit flies Anstreph frterculus (Wied.) nd Certitis cpitt (Wied.) (Dipter: Tephritide), s well s orientl fruit moth Grpholit molest (Busck) (Lepidopter: Tortricide) nd secondry pests like phids, mites nd melybugs (NAVA et l., 2014). Most pech growers still use chemicl control, pplying brod-spectrum insecticides regulrly, such s orgnophosphtes nd pyrethroids, s min control tctics ginst these insects (BOTTON et l., 2011). However, indiscriminte use of insecticides cn dversely ffect nturl enemies in the orchrds, impiring thus the nturl biologicl control besides encourging rise of species lredy under control (ATANASSOV; SHEARER; HAMILTON, 2003). Predtory insects from the fmily Chrysopide nturlly occur in vrious griculturl ecosystems, including pech orchrds (SCHUBER et l., 2008). Among the lcewing species, Chrysoperl extern (Hgen) (Neuropter: Chrysopide) is the most bundnt nd hs been widely studied in the Neotropics due to its high potentil for use in biologicl control progrms (ALBUQUERQUE; TAUBER; TAUBER, 1994). This predtor is notble for regulting popultions of severl phytophgous insects in pech crop res, feeding on eggs nd smll lrve of lepidopterns, mites, phids nd melybugs (FREITAS, 2002; DE BORTOLI et l., 2006). Thus, the mintennce of C. extern popultions in pech orchrds should be consistently considered. To this end, the use of selective pesticides or with low impct on this predtor is of upmost importnce. Therefore, it becomes necessry further surveys on insecticide selectivity to this species. Studies on pesticide selectivity to C. extern hve been crried out in Brzil for severl crops; however, the vst mjority of these studies were mde under lbortory conditions (GODOY et l., 2010; MOURA et l., 2010; VILELA et l., 2010). Concerning pech orchrds, lbortoril studies on pesticide selectivity to C. extern hve been performed for lrvl (CASTILHOS et l., 2013) nd dult (CASTILHOS et l., 2011) stges. Nonetheless, there re no records of selectivity studies to dte in neither semi-field nor field conditions with this species in pech trees, which might be due to the high cost nd difficulty of such studies. It is relevnt to ssess pesticide toxicity on non-trget orgnisms, both in conditions of semi-field or field, s it provides definitive informtion bout the rel impct of product ginst given nturl enemy (THOMSON; HOFFMANN, 2006). In this sense, this study imed t evluting the selectivity of five insecticides, commonly used in pech orchrds, to lrve of the predtor C. extern under semi-field conditions. MATERIAL AND METHODS The biossy ws crried out in n experimentl re belonging to the Federl University of Pelots (Universidde Federl de Pelots UFPel) locted in Cpão-do-Leão-RS, Brzil (31º52' S ltitude, 52º21' W longitude), ccording scientific pproch proposed by Vogt (1994) nd Viñuel, Händel nd Vogt (1996). The lrve of C. extern were obtined from colony kept in lbortory (temperture t 25±1ºC, reltive humidity of 70±10% nd photophse of 14 hours). Ech lrv ws fed on nerly 0.06 g of Angst kuehniell (Zeller) (Lepidopter: Pyrlide) eggs nd dults hd n rtificil diet s described by Vogt et l. (2000). Tble 1 describes the insecticides ssessed under semi-field conditions, which hd shown to be hrmful to C. extern lrve through previous lb study (CASTILHOS et l., 2013). These products re recommended to control orientl fruit moth, fruit flies nd phids in pech growing res (AGROFIT, 2016); they were tested t their highest dosges recommended by mnufcturers for pest control in pech orchrds. As control tretment, only distilled wter ws spryed. Tble 1. Insecticides used in pech orchrds nd tested on lrve of Chrysoperl extern in semi-field biossy. Commercil product Active ingredient Chemicl group D.C. 1 C..i. 2 C.c.f. 3 Decis 25 EC Deltmethrin Pyrethroid Imidn 500 WP Phosmet Orgnophosphte Lebycid 500 Fenthion Orgnophosphte Mlthion 1000 EC Mlthion Orgnophosphte Mtch EC Lufenuron Benzoylure D.C. = Dosge of commercil formul (g or ml 100 L -1 ); 2 C..i. = Concentrtion (%) of ctive ingredient tested; 3 C.c.f. = Concentrtion (%) of the tested commercil formul. 110 Rev. Cting, Mossoró, v. 30, n. 1, p , jn. mr., 2017

3 SELECTIVITY OF INSECTICIDES USED IN PEACH FARMING TO LARVAE OF Chrysoperl extern (NEUROPTERA: R. V. CASTILHOS et l. The insecticides were spryed t the previously mentioned dosges on pech trees of nerly 1.5 m of height through CO 2 -pressurized spryer with uniform flt jet nozzle (Teejet XR110015EVS), until lef runoff, which corresponded to volume of bout 0.4 L spry plnt -1. Tretments consisted of four plnts distributed in rndom block experimentl design. A brrier mde of glvnized steel sheet ( meters) with n opening in the middle through which plnt stem pssed protected ech plnt (Figure 1A). A thin lyer of dry sieved soil ws spred over the glvnized steel sheet. Figure 1. Detils of semi-field biossy with lrve of Chrysoperl extern. (A) Protective brrier composed of glvnized steel sheet round pech plnt; (B) Distribution of bit-crds with eggs of Angst kuehniell for lrvl cpture; (C) Plnt covered with voile-type fbric; (D) Lrve of C. extern cptured on bit-crds. After spry drying (2-h lter), 200 second instr C. extern lrve were relesed on ech plnt, nd shortly therefter, ten crdbords (5 7 cm), contining 400 ± 50 eggs of A. kuehniell (round 4,000 eggs), were plced on tretments to serve s ttrctive trp for lrvl cpturing. Five of them were fixed on soil surrounding tree stem, nd the other five were hung from brnches by clip (Figure 1B), being replced dily until the end of the evlutions. To void predtion by birds or losses by intense winds nd rinflls, the plnts were protected with voile-type fbric (Figure 1C). Four pillrs supported the protective brrier, s displyed in Figure 1A. Ech pillr ws fixed in continer with wter, which ws used to prevent nts nd other insects to climb up the stem nd feed on C. extern lrve nd A. kuehniell eggs. In turn, the protective brrier enbled the lrve relesed on Rev. Cting, Mossoró, v. 30, n. 1, p , jn. mr.,

4 Number of cptured lrve SELECTIVITY OF INSECTICIDES USED IN PEACH FARMING TO LARVAE OF Chrysoperl extern (NEUROPTERA: R. V. CASTILHOS et l. plnts to behve nturlly, moving up nd downwrd long the plnt stem. Counting ws performed dily for the four first dys fter sprying, checking the number of lrve on ech bit-crd with eggs of A. kuehniell (Figure 1D). The lrve were removed from bit-crds using fine-bristle pintbrush, counted nd subsequently relesed bck onto the plnt cnopy, viewing to put them in contct with the pesticide residue gin. The number of cptured lrve per tree of ech tretment ws tken into ccount for insecticide effect clcultion. Such clcultion ws mde through the following formul: E% = 100 x [(C T) / C], wherein E% = Effect (%); C = verge number of lrve cptured in control nd T = verge number of lrve cptured in treted plnts (ABBOTT, 1925). According to the effect (E%), insecticides were rted into toxicity ctegories for semi-field biossys estblished by the Interntionl Orgniztion for Biologicl nd Integrted Control of Noxious Animls nd Plnts (IOBC), which re: 1) hrmless (< 25%); 2) slightly hrmful (25-50%); 3) modertely hrmful (51-75%) nd 4) hrmful (> 75%). Dt regrding the number of cptured lrve per tretment underwent vrince nlysis, nd the mens were compred by the Tukey s test, t 5% probbility, using Winstt softwre (MACHADO; CONCEIÇÃO, 2007). RESULTS AND DISCUSSION Among the evluted insecticides, Figure 2 shows tht deltmethrin, fenthion, mlthion nd phosmet reduced the number of cptured lrve on the first dy fter relese (1 DAR) (F = 6.86, df = 5, p = ). Cptures rnged from 15.3 to 22.5 by tretment with fenthion nd mlthion respectively, showing reduction of more thn 50% compred to control. 60 b Control Deltmethrin c c c bc Fenthion Phosmet Lufenuron Mlthion DAR 2 DAR 3 DAR 4 DAR Figure 2. Averge number (± stndrd error) of Chrysoperl extern lrve cptured during the four-dy tril in pech plnts spryed with insecticides under semi-field conditions. Mens followed by different letters ech dy fter relese (DAR) differ significntly by the Tukey's test t 5% probbility. At 1, 2, 3 nd 4 DAR, 47.3, 23.8, 22.8 nd 13.3 lrve were cptured for tretment with lufenuron, respectively. These verges were not significntly different from those observed in control, which were 49.8, 21.5, 18.3 nd 12.8 lrve collected, respectively (Figure 2). At 2, 3 nd 4 DAR, the number of cptured lrve in tretments with deltmethrin, fenthion, mlthion nd phosmet hd no difference from lufenuron or control (2 DAR: F = 2.32; df = 5; p = 0.085; 3 DAR: F = 1.86; df = 5; p = 0.15; 4 DAR: F = 1.28; df = 5; p = 0.31) (Figure 2). With respect to insecticide effect nd toxicity clssifiction, Tble 2 shows tht the verge number of lrve cptured during the four-dy tril in plnts spryed with the orgnophosphte insecticides fenthion nd phosmet were significntly lower thn control (F = 6.05; df = 5; p < ). 112 Rev. Cting, Mossoró, v. 30, n. 1, p , jn. mr., 2017

5 SELECTIVITY OF INSECTICIDES USED IN PEACH FARMING TO LARVAE OF Chrysoperl extern (NEUROPTERA: R. V. CASTILHOS et l. These forementioned insecticides were clssified s modertely hrmful (clss 3), with n effect of 51.6 nd 61.9% on lrve, respectively. The pyrethroid deltmethrin nd the orgnophosphte mlthion reched similr effect, reducing in pproximtely 43% the cpture of lrve, being therefore clssified s slightly hrmful (clss 2). The insect growth regultor lufenuron did not reduce the verge number of cptured lrve, nd ws considered hrmless (clss 1). Tble 2. Averge number (± stndrd error) of cptured Chrysoperl extern lrve, effect nd IOBC toxicity clss of the ssessed insecticides under semi-field conditions. Tretment D.C. 1 n ± SE* E% 2 C 3 Control ± 4.9 b - - Deltmethrin ± 1.9 bc Fenthion ± 1.5 c Phosmet ± 2.1 c Lufenuron ± Mlthion ± 1.5 bc D.C. = Dosge of commercil formul (g or ml 100 L -1 ); 2 E% (Insecticide effect) = 100 x [(C T) / C], wherein C = verge number of lrve cptured in control nd T = verge number of lrve cptured in treted plnts (ABBOTT, 1925); 3 IOBC toxicity clssifiction for semi-field tril: 1= hrmless (< 25%); 2 = slightly hrmful (25-50%); 3 = modertely hrmful (51-75%); 4 = hrmful (> 75%). * Mens followed by different letters differ significntly by the Tukey's test t 5% probbility. Either the pyrethroid deltmethrin or the orgnophosphtes fenthion, phosmet nd mlthion re fetured by knockdown effect nd, thus, cting fster by cusing symptoms such s shivering, reduced movement, regurgittion nd excessive excretion in insects (HARAMBOURE et l., 2013). Differently, lufenuron interfere in the molting by inhibiting chitin synthesis (ADEL, 2012), which my explin the difference from neurotoxic insecticides t 1 DAR. An insect popultion survivl is ffected by environmentl resistnce, which is responsible for nturl mortlity cused by dverse wether conditions mong others s biotic ctions of prsitoids, predtors nd pthogens, s well s lck or poor qulity of hosts (PETERSON et l., 2009). Therefore, covering the plnts with voile-type fbric (Figure 1C) ws crucil since plyed down wether ction such s rinfll nd winds. Between the first nd the second DAR, rinfll of 22 mm poured down nd the cloth could not void lef wetting but prevented lrve nd bit-crds to suffer direct impct from rindrops. The decresing number of cptured lrve t 2, 3 nd 4 DAR, in ll tretments, my be prtly relted to rinfll, however, evlutions of insecticidl effect on lrve ws not impired, since ll tretments underwent the sme environmentl ctions. The number of lrve collected in control over the four-dy evlution closely resembles tht chieved by Viñuel, Händel nd Vogt (1996) running field biossy conducted in similr mnner to this study, with protective brrier. These uthors collected in the first ctch round 20% from lrve of Chrysoperl crne (Stephens) (Neuropter: Chrysopide) relesed onto untreted pple trees, with decresing rte s the dys pssed. Evluting the effect of nturl pyrethrin-bsed insecticde under field conditions, Viñuel, Händel nd Vogt (1996) found non-hrmful effect ginst lrve of C. crne, nd clssified it s hrmless (clss 1). These uthors climed tht such finding ws due to low persistence of nturl pyrethrin, since they re esily susceptible to photo-degrdtion compred to synthetic ones. Conversely to this study, where deltmethrin ws considered slightly toxic (clss 2) to C. extern, Vogt (1994) confirmed high toxicity of cyfluthrin, lso pyrethroid, to C. crne lrve, rting it s hrmful (clss 4). The sme uthor evluted phosmet nd clssified s hrmless (clss 1) to C. crne, with only 10.5% reduction in lrve cpture, wheres it ws modertely hrmful (clss 3) to C. extern, in the present study. These differences my derive from ctive ingredient intrinsic chrcteristics, whose levels of toxicity my vry within chemicl group, type of formultion, presence of inert nd djuvnt ingredients nd different dosges (KALAMARAKIS; MARKELLOU, 2007). Differences in susceptibility between species cn lso interfere with toxicity of the insecticides in question, s these species hve different enzyme detoxifiction systems. C. crne tolernce to certin pesticides, prticulrly pyrethroids, is ttributed, mong others, to high ctivity of esterse enzymes (MULLIGAN et l., 2010); while for C. extern, the P450 monoxygenses, nother enzyme group, cts jointly with esterses nd provides degree of nturl tolernce to pyrethroids (HARAMBOURE, 2016). Furthermore, the use of different lef substrtes, pple in the study of Vogt (1994), my hve effect on the results. As stted by Zongmo nd Hibin (1997), lef substrte cn influence insecticide toxicity, since ctive ingredient metboliztion nd concentrtion into the leves my vry depending on species intrinsic fetures, for Rev. Cting, Mossoró, v. 30, n. 1, p , jn. mr.,

6 SELECTIVITY OF INSECTICIDES USED IN PEACH FARMING TO LARVAE OF Chrysoperl extern (NEUROPTERA: R. V. CASTILHOS et l. exmple hiriness, roughness nd lef growth rte. Some popultions of lcewings show certin degree of tolernce to neurotoxic insecticides, with no deleterious effects on biotic potentil nd predting bility (PATHAN et l., 2008; PATHAN et l., 2010; HARAMBOURE et l., 2013), which mkes them n importnt choice for progrms where biologicl nd chemicl control re required. Under conditions where sprying of neurotoxic insecticides becomes extremely necessry in pech orchrds, deltmethrin or mlthion re the most rtionl choice for mintennce of C. extern, since these products were the lest hrmful to this predtor lrve mong the neurotoxic insecticides evluted. Likewise to the current study where lufenuron proved hrmless effect, Hrmboure (2016) found high selectivity of the insect growth regultor pyriproxyfen to C. extern, demonstrting selectivity of such clss of insecticides to the referred predtor lrve. According to Thomson nd Hoffmnn (2006), lcewings re extensively exposed to pesticides, thus the use of selective insecticides s stted by selectivity tests of the IOBC contributes to mintining nd preserving these nturl enemies in griculturl ecosystems. Under this bckground, it is essentil to identify selective insecticides to C. extern nd incorporte them into Integrted Pest Mngement progrms (IPM) to ensure this species biologicl control in pech orchrds. Selectivity studies under conditions of semi-field or field, which re ble to provide most relistic informtion on impcts of pesticides ginst nturl enemies, re still scrce, minly due to methodologicl issues. Despite the dvnces brought by the IPM, chemicl control of pest insects in pech orchrds is, in severl cses, still necessry, of which selective ctive ingredients to nturl enemies must be prioritized. This wy, the insect growth regultor, lufenuron, which hs proven to be hrmless to C. extern lrve, should be recommended for Integrted Pest Mngement progrms in pech growing res, iming to preserve such importnt predtor species. CONCLUSIONS Lufenuron is hrmless (clss 1), deltmethrin nd mlthion re slightly hrmful (clss 2), nd fenthion nd phosmet re modertely hrmful (clss 3) to lrve of C. extern under semi-field conditions. The insect growth regultor, lufenuron, must be prioritized to replce neurotoxic insecticides in pech orchrds, seeking to mintin the popultions of C. extern. REFERENCES ABBOTT, W. S. A method of computing the effectiveness of n inseticide. Journl of Economic Entomology, Annpolis, v. 18, n. 1, p , ADEL, M. M. Lufenuron impir the chitin synthesis nd development of Spodopter littorlis Bosid (Lepidopter: Noctuide). Journl of Applied Sciences Reserch, Jordn, v. 8, n. 5, p , AGROFIT. Sistem de Agrotóxicos Fitossnitários. Disponível em: < grofit.gricultur.gov.br/grofit_cons/ principl_grofit_cons>. Acesso em: 11 mi ALBUQUERQUE, G. S.; TAUBER, C. A.; TAUBER, M. J. Chrysoperl extern (Hgen) (Neuropter: Chrysopide): Life history nd potentil for biologicl control in Centrl nd South Americ. Biologicl Control, Montrel, v. 4, n. 1, p. 8-13, ATANASSOV, A.; SHEARER, P. W.; HAMILTON, G. Pech pest mngement progrms impct beneficil fun bundnce nd Grpholit molest (Lepidopter: Tortricide) egg prsitism nd predtion. Environmentl Entomology, Lnhm, v. 32, n. 4, p , BOTTON, M. et l. Bioecologi, monitormento e controle d mripos-orientl n cultur do pessegueiro no Rio Grnde do Sul. Bento Gonçlves: Embrp Uv e Vinho, p. (Circulr técnic, 86). CASTILHOS, R. V. et l. Selectivity of pesticides used in pech orchrds on the lrvl stge of the predtor Chrysoperl extern (Hgen) (Neuropter: Chrysopide). Semin: Ciêncis Agráris, Londrin, v. 34, n. 6, Sup. 1, p , CASTILHOS, R. V. et l. Seletividde de grotóxicos utilizdos em pomres de pêssego dultos do preddor Chrysoperl extern (Hgen, 1861) (Neuropter: Chrysopide). Revist Brsileir de Fruticultur, Jboticbl, v. 33, n. 1, p , DE BORTOLI, S. A. et l. Desenvolvimento e cpcidde predtóri de Chrysoperl extern (Hgen) (Neuropter: Chrysopide) em diferentes press. Revist de Biologi e Ciêncis d Terr, Cmpin Grnde, v. 6, n. 1, p , FREITAS, S. O uso de crisopídeos no controle biológico de prgs. In: PARRA, J. R. P. et l. 114 Rev. Cting, Mossoró, v. 30, n. 1, p , jn. mr., 2017

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