Survey of insect growth regulator (IGR) resistance in house flies (Musca domestica L.) from southwestern Turkey

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1 Vol., no. Journl of Vector Ecology 9 Survey of insect growth regultor (IGR) resistnce in house flies (Musc domestic L.) from southwestern Turkey Huseyin Cetin, Fedi Erler, nd til Ynikoglu kdeniz University, Fculty of rts nd Science, Biology Deprtment 758 ntly, Turkey kdeniz University, Fculty of griculture, Plnt Protection Deprtment 77 ntly, Turkey Received 8 ugust 9; ccepted Septemer 9 BSTRCT: Insect growth regultors (IGRs) re currently the fstest-growing clss of insecticides, nd in Turkey these products represent new pproch to pest control. In recent yers, severl IGRs were lso registered for the control of the house fly, Musc domestic L. (Dipter: Muscide), in Turkey. field survey ws conducted in the summers of 6 nd 7 to evlute resistnce to some griculturlly nd mediclly used IGRs on house flies from livestock frms nd grge dumps in the greenhouse production res (Merkez, Kumluc, Mnvgt, nd Serik) of ntly province (Southwestern Turkey). The results of lrvl feeding ssy with technicl difluenzuron, methoprene, novluron, pyripoxyfen, nd triflumuron indicte tht low levels (RF<-fold) of resistnce to the IGRs exist in the house fly popultions from ntly province. Exceptions, however, were two popultions, Guzoren nd Topts, from the Kumluc re which showed moderte resistnce to difluenzuron with.8-fold in 6 nd.-fold in 7, respectively. We found sustntil vrition in susceptiility of field-collected house fly popultions from yer to yer nd from product to product. We generlly oserved n increse in resistnce t mny loclities smpled from 6 to 7. The implictions of these results to the future use of IGRs for house fly control re discussed. It will e criticlly importnt to continue monitoring efforts so tht pproprite steps cn e tken if resistnce levels strt to increse. Journl of Vector Ecology (): Keyword Index: House fly, insect growth regultor, Musc domestic, resistnce, Turkey. INTRODUCTION The house fly, Musc domestic L. (Dipter: Muscide), is one of the most common flies where people gther for work nd livelihood. It is potentil vector of more thn different disese orgnisms hrmful to oth humns nd nimls, including protozons, cteri, virus, nd fungi (Greenerg 97, Pndin nd sumth, Clvel et l., Rjendrn nd Pndin ). The diseses trnsmitted y Musc species, including M. domestic, cn include enteric infections (such s dysentery, dirrhe, typhoid, choler, nd certin helminth infections), eye infections (such s trchom nd epidemic conjunctivitis), poliomyelitis, nd certin skin infections (such s yws, cutneous diphtheri, some mycoses, nd leprosy) (Greenerg 97, Oliveir et l. 6). Trnsmission tkes plce when the fly mkes contct with people or their food (Pndin nd sumth ). The control of house flies in Turkey generlly depends on lrvicide tretments of reeding plces comined with strtegic use of neurotoxic insecticides ginst dult house flies. Orgnophosphte nd crmte its nd nonpersistent pyrethroid erosol sprys re registered in Turkey for the ltter use nd re still effective ginst house flies. Over the lst decde, there hs een growing reliztion tht lternte methods to synthetic chemicl control need to e considered. More recently, severl insect growth regultors (IGRs) hve een registered for use in house fly mngement progrms nd IGR-sed lrvicides re ecoming more populr thn the others. These include compounds tht ffect molting nd metmorphosis y mimicking juvenile hormone (JH gonists) or usully ntgonizing JH ctivity (ecdysteroid gonists), or with chitin synthesis inhiitors y interfering with cuticle formtion (Smet et l. 99, Oerlnder et l. 99, Oerlnder et l. 997). None of them is expected to hve hrmful effects on wildlife, humns, or the environment when used s specified on the product lels (Oerlnder et l. 997). In the lst decde, the use of IGRs hs lso een one of the est lterntives to the conventionl chemicl insecticides used ginst mny griculturl pests, especilly greenhouse pests, in Turkey. ntly (in southwestern Turkey) is the leding greenhouse production province with 5% of totl greenhouse re in Turkey (nonymous 9). Its dominnt position is explined y climtic fctors nd y technologicl nd infrstructure dvntges. Insecticide resistnce is mjor prolem in control progrms for mediclly nd griculturlly importnt insects. The presence of widespred resistnce results in the spred nd increse of pesticide usge cusing environmentl nd helth prolems. This lso cuses mjor prolems for griculturl production nd for the control of vectororne diseses. Therefore, resistnce mngement strtegies should e developed in order to set limittion on the usge of the sme group of pesticides. Erly detection of resistnce is considered criticl for the implementtion of successful resistnce mngement strtegies (Leeper et l. 986,

2 Journl of Vector Ecology Decemer 9 Kristensen et l. ). Throughout the world, house flies hve developed resistnce to virtully every insecticide used ginst them nd insecticide resistnce in the house fly is glol prolem (Hrris et l. 98, Georghiou nd Mellon 98, Scott et l. 989, Kufmn et l. 6, Decutis et l. 7, cevedo et l. 9). The evolution of resistnce to IGR insecticides ws not considered to e likely (Willims 967). However, vrious studies hve shown tht resistnce cn evolve in response to this chemicl group, especilly if the selection pressure is sufficiently strong (Cerf nd Georghiou 97, Dyte 97, Keiding et l. 99, Keiding 999). Regionl ssessment of susceptiility of locl popultions of M. domestic to different insecticides cn yield informtion out house fly control progrms tht use suitle insecticides nd cn minimize insecticide resistnce. Therefore, the im of the present study ws to survey the IGR resistnce level of house fly popultions from different loclities in the greenhouse production res of Merkez, Kumluc, Mnvgt, nd Serik locted in ntly province ginst some commonly used IGRs. MTERILS ND METHODS Insecticides The lrvicides used in the iossy were % difluenzuron (Delphin SC; Belg Chem. Corp., nkr, Turkey), 5% methoprene (ltosid SC; Biosv Chem. Corp., nkr, Turkey), % novluron (Oscr EC; Byer, İstnul, Turkey), % pyripoxyfen (dmirl EC; Sumitomo, ntly, Turkey), nd 8% triflumuron (Strcide SC; Byer, İstnul, Turkey). The concentrtions used for iossys were.,.,.,.5,, 5,, 5, nd 5 ppm, respectively. First, stock solution t ppm ws prepred in distilled wter for ech lrvicide, nd then the lower concentrtions were prepred y seril dilution of ech stock solution. Smpling sites nd field popultions Field popultions of house flies were collected y using sweep nets from livestock frms nd grge dumps in the greenhouse production res of Merkez, Kumluc, Mnvgt, nd Serik in the summers of 6 nd 7. In these res, the IGR insecticides such s difluenzuron, novluron, pyripoxyfen, nd triflumuron hve een widely used for six to eight yers ginst greenhouse pests nd for two yers ginst M. domestic. House fly dult smples were collected from five rndomly selected loclities in ech of the res: Topculr, Vrsk, Yurtpinr, Kepez, nd Ciglik in the center re of ntly city (Merkez); Guzoren, Topts, Kspcyi, Hciveliler, nd Kvk in the Kumluc re; Celtikci, sgi isiklr, Merkez, Tsgil, nd Colkli in the Mnvgt re; nd Cumli, Merkez, Gedik, Urundu, nd Cndir in the Serik re. The loclities in ech re were more thn five km prt from ech other nd dispersl of house flies etween the popultions ws not expected to occur. The collected flies were trnsported in fine muslin cges ( 6 cm) including cue sugr nd wetted cotton pds to the Toxicology Lortory within four to six h. One smple consisted of - house flies. The collected house flies were incuted for two h t º C to void possile entomopthogenic infections. Lortory strin The World Helth Orgniztion strin (WHO ss ) developed nd mintined t the WHO Collorting Lortory t the Deprtment of Biology, kdeniz University, ws used s the susceptile stndrd reference strin for iossys. Biossys The femles of field-collected house flies nd the susceptile stndrd reference strin were llowed to ly eggs on cotton pds wetted with milk in the lortory. Lrvicide iossys were performed with to 6-h-old lrve. The iossy test for the lrve involved feeding of lrvicides crried out ccording to the method descried y Kristensen nd Jespersen () nd Cetin et l. (6) with some modifictions. To test the toxicity of lrvicides, portions of rtificil lrvl rering medium (one portion: g whet rn, g ker-yest, 5 ml mlt extrct, 5 ml whole milk, nd 5 ml wter) were treted with different concentrtions of ech test lrvicide. Twenty-five grms of medium were put in continer ( ml polystyrene cups) nd treted with.5 ml of wter contining lrvicide or wter lone nd then mixed into the medium with glss sptul. Twenty-five to 6-h-old lrve were plced in rering continers. Four replictes of twenty-five lrve were used for ech concentrtion level of ech lrvicide. The numer of emerging flies ws recorded during the threeweek test period nd oservtions continued until no live lrve were found. The lrvicidl effect ws determined s the percentge of emerging house flies on the sis of the numer of introduced lrve. ll lrvicidl ssys were mde in triplicte for oth field-collected strins nd the susceptile stndrd reference strin. ll tests were run t : (L:D) photoperiod, 6 ± % RH, nd 6 ± C. The full lrvicidl iossy ws performed in triplicte t eight different concentrtions (three times 5 lrve t ech concentrtion of lrvicide) nd control without lrvicide to monitor ckground mortlity. Resistnce fctor, RF, ws clculted y division of the determined LC 5 y the stndrd reference LC 5 (Tle ). Sttisticl nlysis Percentge mortlity oserved in the control ws sutrcted from tht oserved in the tretments (ott 95). The dt re presented s n nlysis of vrince using the Duncn s Multiple Rnge Test (DMRT) (SPSS.) t the P.5 level of significnce (SPSS 999). The LC 5 vlues were clculted using proit nlysis progrm (US EP, 999). The resistnce fctor vlues were ctegorized ccording to Rupes et l. (976) into four groups: low (RF<), moderte (RF=-), high (RF=-6) nd very high (RF>6).

3 Vol., no. Journl of Vector Ecology Tle. LC 5 vlues (ppm) of WHO sensitive Musc domestic popultions tht were used for comprison with the fieldcollected popultions from the res smpled in ntly province. Comprison Difluenzuron Methoprene Triflumuron Novluron Pyriproxyfen 7 First three loctions ntly (Topculr, Vrsk, Yurtpinr) Serik (Cumli, Gedik, Merkez) Mnvgt (Celtikci, sgi Isikler, Merkez) Kumluc (Guzoren, Topts, Kspcyi). (.-.).8 (.6-.7).5 (.-.7).9 (.-.89). (.7-.) 7 Lst two loctions ntly (Kepez, Ciglık) Serik (Urundu, Merkez) Mnvgt (Tsgil, Colkli) Kumluc (Hciveliler, Kvk).8 (.-.7). (.-.9). (.-.5).57 (.-.78).7 (.6-5.9) 8 First three loctions ntly (Topculr, Vrsk, Yurtpinr) Serik (Cumli, Gedik, Merkez) Mnvgt (Celtikci, sgi Isikler, Merkez) Kumluc (Guzoren, Topts, Kspcyi).9 (.7-.).9 (.7-.). (.6-.5).8 (.-.). (.7-.78) 8 Lst two loctions ntly (Kepez, Ciglık) Serik (Urundu, Merkez) Mnvgt (Tsgil, Colkli) Kumluc (Hciveliler, Kvk).8 (.9-.58).5 (.6-.6). (.-.97).7 (.5-.97).7 (.76-.8) RESULTS Low levels (RF<-fold) of resistnce to the IGRs exist in the house fly popultion from ntly province, with the exception of two popultions, Guzoren nd Topts, from the Kumluc re tht showed moderte resistnce to difluenzuron with.8-fold in 6 nd.-fold in 7, respectively (Tle ). lthough popultions collected from ll the study res, except for Serik, showed similr susceptiility to the IGRs tested in oth yers, house flies collected in the second yer of the study (7) generlly hd higher RF vlues thn those collected in the first yer (6). The Kumluc re hd higher levels of resistnce for ll the lrvicides tested thn the rest of the res smpled. The highest RF vlues were found for difluenzuron in the Guzoren (.8-fold in 6) nd Topts (.-fold in 7) popultions from the Kumluc re (Tle ). With the exception of novluron, n increse ws oserved in the men RF vlues t ll the loclities of the Merkez re of ntly province from 6 to 7. When the men RF vlues for ll the lrvicides were compred ech other, there were no significnt differences mong the lrvicides in ech of the two yers (Figure ). For the Serik re, the men RF vlues for difluenzuron decresed in the second yer, wheres those for the other lrvicides incresed. In the first yer of the study, the RF vlue for difluenzuron ws sttisticlly higher thn those for ll the other lrvicides (P.5), wheres in the second yer there were no significnt differences mong the RF vlues for ll the lrvicides (Figure ). For ll the lrvicides tested

4 Journl of Vector Ecology Decemer 9 Tle. LC 5 (ppm) nd resistnce fctor (RF) vlues of field-collected Musc domestic popultions from the res smpled in ntly province. Popultions Smpling Loctions Insect Growth Regultors Difluenzuron Methoprene Triflumuron Novluron Pyriproxyfen LC 5 RF Topculr Vrsk ntly Yurtpinr Kepez Ciglik Cumli Gedik Serik Merkez Urundu Cndır Celtikci şgı Isiklr Mnvgt Merkez Tsgıl Colklı Guzoren Topts Kumluc Kspcyı Hciveliler Kvk

5 Vol., no. Journl of Vector Ecology in the Mnvgt re, higher RF vlues were oserved in the second yer compred to the first yer. However, no significnt differences were found mong the RF vlues for ll the lrvicides in oth yers. In the Kumluc re, the RF vlues for ll the lrvicides were higher in 7 thn in 6 (Figure ). In oth yers, the RF vlues for difluenzuron were sttisticlly higher thn those for the other lrvicides (P.5). When the res were compred in terms of men RF vlues for ech of the lrvicides, the highest men RF vlue for difluenzuron ws found in the Kumluc re followed y Serik, Mnvgt, nd ntly-merkez res (Figure ). In oth yers, there were no significnt differences mong the men RF vlues for difluenzuron in ll the res smpled. For novluron, the highest men RF vlue ws oserved in the Mnvgt re in 6 nd in the Kumluc re in 7. Except for the Kumluc re, no significnt differences were found etween the RF vlues for novluron in oth yers. For triflumuron, the highest men RF vlues were oserved in the Kumluc re in oth yers. Except for this re, there were no significnt differences etween the RF vlues for triflumuron in ll other res. For methoprene nd pyriproxyfen, the highest men RF vlues were oserved in the Kumluc re; however, there were no significnt differences in ll the res smpled in terms of men RF vlues in oth yers. DISCUSSION To improve the use of existing insecticides nd dely the onset of resistnce resulting in tretment filures, it is importnt to use regulr surveys to estlish the extent of insecticide resistnce, even for species with n extensive resistnce history. Regulr surveys of resistnce to insecticides of interest in reltion to house fly control in Turkey hve een crried out for mny yers y collecting urn lrvl house flies in vrious prts of the country nd testing the resistnce in the offspring. The insecticidl effect hs usully een iossyed y topicl ppliction with field strins of M. domestic nd with susceptile reference strin. House fly resistnce hs een previously reported in Turkey for orgnochlorine, orgnophosphte, crmte, nd pyrethroid insecticides, ut so fr there hs een no report on IGR resistnce in Turkish house fly popultions (Tylor 98, Sisli et l. 98, Cglr 99, Ymnel nd Ckır, kiner nd Cglr 6). This study ws the first to exmine the IGR resistnce of Turkish house fly popultions. The IGR insecticides hve een used for house fly control since nd for greenhouse pest control since the lte 99s in ntly province, nd their usge tody is more common thn the other groups of insecticides. In this survey we found low levels (RF<-fold) of resistnce in field popultions of M. domestic from southwestern Turkey (ntly province) towrd IGR insecticides, except for two popultions, Guzoren nd Topts, from the Kumluc re which exhiited moderte resistnce to difluenzuron with.8-fold in 6 nd.-fold in 7, respectively. House flies collected in the second yer of the study (7) showed similr susceptiility to the IGRs tested, compred with the first yer (6). One exception ws the Kumluc popultions, which hd significntly higher RF vlue for novluron in 7 (.8), reltive to 6 (.6). This is consistent with the intensive use of IGR insecticides, especilly those included in the present study, t this greenhouse production re strting in 998 nd my e n indiction tht IGR resistnce is evolving t this re. Monitoring IGR resistnce t this re should e given priority. Unfortuntely, ecuse of finncil limittions, the numer of popultions from this re tht we were le to monitor ws limited to five. Unlike our findings, Keiding (999) reports tht two IGRs, difluenzuron nd cyromzine, hve een widely used since 979 nd 988, respectively, for fly control on livestock frms in Denmrk, either y direct ppliction to reeding sites, mnure, grge, etc., or s n dmixture in feed for poultry or pigs, nd regulrly monitoring of susceptiility to these IGRs hs not shown indiction of resistnce development. However, there re reports showing tht the use of the IGR insecticides, difluenzuron nd cyromzine, mixed into feed hs resulted in the development of moderte to high resistnce to these compounds, nd susequent complints of control filure(s) in the U.S.. nd Jpn (Iseki nd Georghiou 986, Bloomcmp et l. 987, Shen nd Plpp 99). Resistnce to difluenzuron nd cyromzine ws lso oserved y Kristensen nd Jespersen () in survey of resistnce in Dnish field popultions of M. domestic. There is control filure for ll other insecticides used for house fly control in Turkey, nd mny compounds re still eing used y locl uthorities. Resistnce is high nd seems to e stle for these compounds (Sisli et l. 98, Cglr 99, kiner nd Cglr 6). lthough high resistnce in dult flies to orgnophosphtes nd pyrethroids does not usully confer cross-resistnce to the vrious IGRs (Keiding et l. 99, Kristensen nd Jespersen ), severl studies report tht there hs een cross-resistnce etween orgnophosphorus compounds nd some juvenile hormone mimics, e.g., methoprene (Cerf nd Georghiou 97, 97). In tht cse, the use of conventionl insecticides must e restricted efore more serious prolems occur. However, there is n urgent need for further monitoring nd the estlishment of more effective progrms tht cover ll spects of the resistnce prolem. cknowledgments The uthors re thnkful to the Scientific nd Technologicl Reserch Council of Turkey (TÜBİTK) nd the Scientific Projects dministrtion Unit of kdeniz University (ntly, Turkey) for their finncil support.

6 Journl of Vector Ecology Decemer 9 ntly/merkez RF vlues,5,5,5 Difluenzuron Novluron Triflumuron Methoprene Pyriproxyfen,5 Serik RF vlues,5,5,5 Difluenzuron Novluron Triflumuron Methoprene Pyriproxyfen,5 Mnvgt RF vlues,5,5 Kumluc RF RF vlues 8 6 Difluenzuron Novluron Triflumuron Methoprene Pyriproxyfen B Difluenzuron Novluron Triflumuron Methoprene Pyriproxyfen B B B Figure. The men RF vlues of house fly popultions from the res smpled in ntly province in lrvicidl feeding iossys with the insect growth regulting insecticides in 6 nd 7. The sme lower-cse letters on the rs showing the lrvicides re not significntly different in 6 (p>.5). The sme cpitl letters on the rs showing the lrvicides re not significntly different in 7 (p>.5).

7 Vol., no. Journl of Vector Ecology 5 Difluenzuron RF vlues 8 6 ntly Serik Mnvgt Kumluc Novluron RF vlues 5,5,5,5,5,5 ntly Serik Mnvgt Kumluc Triflumuron RF vlues,5,5,5,5,5 ntly Serik Mnvgt Kumluc Figure. Resistnce rtios (RF) of house fly popultions from the smpling res of ntly province to the insect growth regulting insecticides in 6 nd 7. Methoprene RF vlues,5,5,5,5 ntly Serik Mnvgt Kumluc 6 5 Pyriproxyfen RF vlues ntly S erik Mnvgt K umluc

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