Colorado Potato Beetle Resistance to Insecticides

7/26/2019 Colorado Potato Beetle Resistance to Insecticides

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Colorado Potato Beetle Resistance to

Insecticides

Andrei Alyokhin, Mitchell Baker , David Mota-Sanchez, Galen Dively,and EdwardGrafius

This peer-refereed invited review article has been first published in the December, 200,

issue of the !merican "ournal of Potato Research #$olume %, &umber ', Pa(es )*%-

+). The ori(inal publication is available at www.sprin(erlin/.com. Reproduced with

permission of the publisher.

!BTR!CT

The Colorado otato !eetle, Leptinotarsa decemlineata "Say#, is widely re$arded asthe %ost i%ortant insect defoliator of otatoes& 'ts current ran$e covers a!out ()%illion k%* in +orth A%erica, Euroe, and Asia and continues to eand& Thisinsect has a co%licated and diverse life history, which is well-suited to a$ricultural

environ%ents, and %akes it a co%le and challen$in$ est to control& Disersal,closely connected with diaause, feedin$, and reroduction, allow the Colorado otato !eetle to e%loy !et-hed$in$ reroductive strate$ies, distri!utin$ itsoffsrin$ in !oth sace "within and !etween fields# and ti%e "within and !etweenyears#&

The Colorado otato !eetle layed a lar$e role in creatin$ the %odern esticideindustry, with hundreds of che%icals tested a$ainst it& .i$h selection ressure,to$ether with natural roensity to adat to toic su!stances, eventually resulted ina lar$e nu%!er of insecticide-resistant Colorado otato !eetle oulations& Since

the %iddle of the last century, the !eetle has develoed resistance to /* differentco%ounds !elon$in$ to all %a0or insecticide classes& 1esistance levels vary$reatly a%on$ different oulations and !etween !eetle life sta$es, !ut in so%ecases can !e very hi$h "u to *,222-fold#&

3nown %echanis%s of Colorado otato !eetle resistance to insecticides includeenhanced %eta!olis% involvin$ esterases, car!oylesterases and %onooy$enases,and tar$et site insensitivity, as well as reduced insecticide enetration and increasedecretion& There is also so%e evidence of !ehavioral resistance& 1esistance%echanis%s are so%eti%es hi$hly diverse even within a relatively narrow$eo$rahical area& 1esistance is usually inherited as an inco%letely do%inant orinco%letely recessive trait, with one or several $enes involved in its

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http://dx.doi.org/10.1007/s12230-008-9052-0

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deter%ination& Because of leiotroic effects of resistant alleles, insecticide-resistant !eetles often have reduced relative fitness in the a!sence of insecticides&

1otatin$ different classes of insecticides and reducin$ insecticidal ressure on est oulations !y rovision of te%oral and satial refu$es fro% eosure to toinshave !een roosed to delay evolution of resistance& .owever, insecticideresistance in this insect will likely re%ain a %a0or challen$e to the est control

ractitioners& Still li%ited understandin$ of !eetle !iolo$y, its flei!le life history,and $rower reluctance to adot so%e of the resistance %ana$e%ent techni4uescreate i%edi%ents to successful resistance %ana$e%ent& 5verco%in$ theseo!stacles is not an easy task, !ut it will !e crucial for sustaina!le otato

roduction&

C11R!D1 P1T!T1 B33T3 ! !& I&T3R&!TI1&! 4P3RP3T

Colorado otato !eetle, Leptinotarsa decemlineata "Say#, is a leaf !eetle"Coleotera6 Chryso%elidae# native to the southwestern 7nited States and Meico&'t was first collected in (8(( !y Tho%as +uttall and then descri!ed !y Tho%as Sayin (8*9 ":ac4ues (;88#& <ild oulations were o!served feedin$ on

!uffalo!ur,Solanum rostratum Dunal& and several related secies in the fa%ilySolanacea& =or %ore than four decades after its ori$inal discovery, the !eetle wasof little ractical si$nificance& .owever, the situation chan$ed dra%atically afterthe area of its ori$inal distri!ution was settled !y far%ers of Euroean descent& The

settlers !rou$ht with the% otato, Solanum tuberosum >&, and started to cultivate itover considera!le acrea$es& 7nfortunately, the otato roved to !e a hi$hlysuita!le host lant for L. decemlineata, and the !eetles 4uickly switched to feedin$on the new and a!undant host lant "Casa$rande (;8?@ :ac4ues (;88@ <e!er *22#&

The first %a0or Colorado otato !eetle out!reak occurred in (8/; on otato fieldsa!out (22 %iles west of 5%aha, +e!raska ":ac4ues (;88#& The su!se4uenteansion in !eetle $eo$rahic ran$e was so%ewhat %ind-!o$$lin$, with !eetlesreachin$ the Atlantic coast of the 7&S& and Canada !efore (882 "Casa$rande (;8?#&The first Euroean oulation was esta!lished in =rance in (;**& By the end of the*2th century, the est had !eco%e a ro!le% all over Euroe, in Asia Minor, 'ran,Central Asia, and western China ":olivet (;;(@ <e!er *22#& 'ts current ran$ecovers a!out () %illion k%* on two continents and continues to eand "<e!er*22#& otentially, the !eetle could sread to te%erate areas of East Asia, the'ndian su!continent, South A%erica, Africa, +ew ealand, and Australia "lasova(;?8@ <orner (;88@ :olivet (;;(@ <e!er *22#&

Currently, the Colorado otato !eetle is widely re$arded as the %ost i%ortantinsect defoliator of otatoes& 't also causes si$nificant da%a$e to to%ato and

e$$lant& 5ne !eetle consu%es aroi%ately 92 c%* of otato leaves durin$ thelarval sta$e ">o$an et al& (;8/@ =erro et al& (;8/#, and close to an additional (2 c%*



of folia$e er day as an adult "=erro et al& (;8/#& 'n addition to i%ressive feedin$rates, the Colorado otato !eetle is also characterized !y hi$h fecundity, with onefe%ale layin$ 22-822 e$$s ".arcourt (;?(#& 'f left uncontrolled, the !eetles canco%letely destroy otato cros&

I53 6IT1R7

The Colorado otato !eetle has a co%licated and diverse life history, which iswell-suited to a$ricultural environ%ents, and %akes it a co%le and challen$in$

est to control& Disersal, closely connected with diaause, feedin$, andreroduction, allow this insect to e%loy !et-hed$in$ reroductive strate$ies,distri!utin$ its offsrin$ in !oth sace "within and !etween fields# and ti%e "within

and !etween years#& As a result, the risk of catastrohic losses of offsrin$ due toinsecticides or cro rotation is di%inished "Sol!reck (;?8@ oss and =erro (;;2#&

The Colorado otato !eetle is caa!le of %ovin$ !oth !y fli$ht and !y walkin$"Boiteau et al& *22#& Adults start walkin$ i%%ediately after they e%er$e fro%

uation in the soil "oss and =erro (;;2# and can travel several hundred %eters&<alkin$ seed is the hi$hest on !are $round and decreases with the increasin$density of ve$etation "+$ and >asho%! (;8#& Adult !eetles need to feed for /-(2days after eclosion fro% uae to co%lete fli$ht %uscle develo%ent "oss and=erro (;;2@ an$ (;;9@ <e!er and =erro (;;)#, and then they can easily fly several

kilo%eters "<e!er and =erro (;;9#& =li$ht initiation is stron$ly related to airte%erature and solar insolation "Cario and Grafius (;;2#, and $iven favora!lewind direction the !eetles %ay !e a!le to fly over (22 k% "<iktelius (;8(#& The

!eetles also fly over short distances, distri!utin$ e$$s within the host ha!itat and insearch of %ates "oss and =erro (;;2#&

The Colorado otato !eetle overwinters in the soil as adults& After diaause isinduced !y a short-day hotoeriod "de 3ort (;;2#, the !eetles %ay enter the soilfor diaause in the otato field or %ove towards field ed$es !y fli$ht and !ywalkin$, resu%a!ly orientin$ towards tall ve$etation co%%on in hed$erows "ossand =erro (;;2@ <e!er and =erro (;;@ =rench et al& (;;#& 7on arrival tooverwinterin$ sites, re-diaause %i$rants i%%ediately !urrow into the soil todiaause "oss and =erro (;;2#, and their fli$ht %uscles under$o si$nificantde$eneration "Ste$wee et al& (;)#& Althou$h in so%e areas the %a0ority of !eetlesa$$re$ate in over$rown areas ad0acent to fields where they have sent the revioussu%%er "<e!er and =erro (;;@ =rench et al& (;;#, a su!stantial nu%!er !urrowinto the soil directly in the field "=rench et al& (;;#&

1efractory hase of the diaause, durin$ which the !eetles do not react to the

chan$e in environ%ental conditions, lasts for aroi%ately %onths& After that,the !eetles resond to elevation of te%eratures a!ove (2FC !y e%er$in$ fro% the



soil "de 3ort (;;2#& The !eetles usually accu%ulate /2-*/2 de$ree-days "DD(2,(2FC !ase te%erature# !efore they aear on the soil surface "an$ (;;9@ =erro etal& (;;;#& Males and fe%ales ter%inate their diaause si%ultaneously "an$ (;;9@=erro et al& (;;;#, and re4uire only )2-82 DD(2 !efore they are a!le to %ate "=erroet al& (;;;#& A certain roortion of overwinterin$ !eetles %ay re%ain in the stateof uninterruted etended diaause for two years "'sely (;/@ Trouvelot (;)@<e$orek (;/? a,!@ 7shatinskaya (;)*, (;))#& 'n the western 7kraine, 2&9-)&/ of

!eetles overwinterin$ in sandy soils re%ained dor%ant for two years, !ut all !eetlesoverwinterin$ in clay soils e%er$ed after the first winter "7shatinskaya (;)*,(;))#& Si%ilarly, !etween 2-?&* of !eetles in ustate +ew ork e%er$ed after%ore than one winter in dor%ancy "Tau!er and Tau!er *22*#& 'ncidence of

rolon$ed diaause was even hi$her in <ashin$ton State, where ()-*( ofoverwinterin$ adults e%er$ed after two winters, and u to * e%er$ed after threewinters "Biever and Chauvin (;;2#&

After e%er$ence fro% the soil, overwintered Colorado otato !eetles colonize otato fields !oth !y fli$ht and !y walkin$ "oss and =erro (;;2#& The !eetles donot start flyin$ until they accu%ulate (/2-*22 DD(2 "a%ount re4uired for fli$ht%uscle re$eneration, an$ (;;9#, and !eetle fli$ht is stron$ly encoura$ed !y thea!sence of food "Cario and Grafius (;;2@ =erro et al& (;;(@ <e!er and =erro(;;)@ =erro et al& (;;;@ !ut see MacHuarrie and Boiteau *22#& 'f the fields arerotated, the !eetles are a!le to fly u to several kilo%eters to find a new host ha!itat"=erro et al& (;;(@ <e!er and =erro (;;)#& .owever, this is not a directed fli$httoward new fields and nu%!ers of !eetles arrivin$ in new fields are $reatly reduced

and arrival is delayed "<eisz et al& (;;)#& 5nce they have colonized the field, theoverwintered !eetles first feed and then oviosit within /-) days "=erro et al& (;8/@=erro et al& (;;(#&Deendin$ on te%erature, develo%ent fro% e$$ to adult takes !etween (9-/)days "de <ilde (;98@ <al$en!ach and <y%an (;89@ >o$an et al& (;8/@ =erro et al&(;8/#& The fastest develo%ent occurs !etween */-*IC and aears to differa%on$ oulations of different $eo$rahic ori$ins& The larvae are caa!le of

!ehavioral ther%ore$ulation via %ovin$ within lant canoies "May (;8(@ >actinand .olliday (;;9#, thus oti%izin$ their !ody te%erature co%ared to the

a%!ient te%erature& Diaause is facultative, and the !eetles can have !etween oneand three overlain$ $enerations er year& The %a0ority of adults die durin$ thesecond su%%er of their lives& .owever, a certain roortion of overwintered

!eetles enter the second diaause in the followin$ winter "'sely (;/@ de <ilde(;)*@ :er%y and Sarin$er (;//@ Minder and etrova (;))#& As %any as */ of theoverwintered oulation %ay enter the second diaause "Minder and etrova(;))#, !ut overwinterin$ and srin$ %ortality a%on$ such !eetles is very hi$h"'sely (;/@ Minder and etrova (;))#&

The !eetleJs %atin$ !ehavior is stron$ly directed towards %ai%izin$ $enetic

varia!ility of its ro$eny& After accu%ulatin$ at least 9DD(2 since e%er$encefro% uae "Alyokhin and =erro (;;;a#, !oth %ales and fe%ales erfor% %ultile



coulations with different artners "Szentesi (;8/#& <hen a su%%er $enerationfe%ale %ates to two different %ales, ser% recedence is inco%lete, with the first%ale fertilizin$ *8-98 of the e$$s "Boiteau (;88a@ Alyokhin and =erro (;;;!@1oderick et al& *22#& =e%ales do not usually start oviositin$ until theyaccu%ulate at least /( DD(2 since e%er$ence fro% uae "Alyokhin and =erro(;;;a#& ost-diaause fe%ales can lay e$$s usin$ ser% fro% the re-diaause%atin$ the revious fall@ however, the nu%!er of offsrin$ roduced !y suchfe%ales is lower co%ared to srin$-%ated fe%ales "=erro et al& (;;(@ Baker et al&*22/#& Therefore, !eetles usually %ate a$ain after diaause ter%ination in thesrin$& Matin$ starts !efore !eetles leave for the host ha!itat, with at least half ofthe oulation %atin$ within the overwinterin$ sites "=erro et al& (;;;#& Ser%fro% srin$ %atin$ tyically takes recedence over overwintered ser% fro% the

revious yearKs %atin$ "Baker et al& *22/#&

Matin$ status affects !eetle fli$ht activity& 7nlike fe%ales fro% a nu%!er of otherinsect secies ":ohnson (;);@ Din$le (;8/#, $ravid Colorado otato !eetle fe%alescontinue to dislay a considera!le a%ount of fli$ht activity "=erro et al& (;;;@Alyokhin and =erro (;;;a#, allowin$ the% to distri!ute e$$s within and !etweenfields& +evertheless, they still fly si$nificantly less than un%ated fe%ales"Alyokhin and =erro (;;;a#, ro!a!ly !ecause !oth %i$ration and reroduction are

hysiolo$ically de%andin$ for fe%ales, and these two rocesses are known tointerfere with each other "1ankin et al& (;8)#& Contrary to %ated fe%ales, %ated%ales increase their fli$ht activity, increasin$ the nu%!er of coulations withdifferent %ates "Alyokhin and =erro (;;;a# and $enetic diversity of their offsrin$

"McCauley and 1eilly (;89#& 7nlike fli$ht of the su%%er-$eneration !eetles,fli$ht of ost-diaause !eetles is not affected !y their %atin$ status "=erro et al&(;;;#&

C638IC! C1&TR1 !&D I&3CTICID3 R3IT!&C3

The Colorado otato !eetle has !een credited with !ein$ lar$ely resonsi!le forcreatin$ the %odern insecticide industry "Gauthier et al& (;8(#& Since (8)9,hundreds of co%ounds were tested a$ainst this est, and alication e4ui%entwas secifically invented to aid their delivery "Gauthier et al& (;8(#& The earlyche%icals of choice were arsenicals, such as aris $reen and lead arsenate, and, to as%aller de$ree, !otanical rotenone "Brown (;/(#& The !eetles were also one of theinitial tar$ets for DDT alications, with initial alications as early as (;;".itchner (;/*@ Gauthier et al& (;8(#& Currently, insecticides still re%ain thefoundation of the Colorado otato !eetle control on co%%ercial otato far%s&More than 2 active in$redients are currently re$istered for use a$ainst this est inthe 7nited States "Ta!le (#&



Table . Insecticides re(istered for the Colorado potato beetle control arran(ed b9 the mode of action

developed b9 the Insecticide Resistance !ction Committee #200.

:roup ub(roup8ode of

!ctionChemical (roup Trade na

( A Acetylcholineesteraseinhi!itors

Car!a%ates Car!aryl,car!ofuran%etho%yl,oa%yl

B 5r$anohoshates Azinhos-%ethyl,di%ethoatedisulfoton,ethoro,%alathion,%etha%ido

arathion-

%ethyl, h hos%et

* A GABA-$atedchloridechannelanta$onists

Cyclodiene or$anochlorines Endosulfa

Sodiu%channel%odulators

yrethroids, yrethrins Cyfluthrin,delta%ethr esfenvaler

er%ethrin

9 A +icotinicAcetylcholinerecetor

a$onists L

+eonicotinoids Aceta%ir dinotefurai%idaclor

thia%etho



anta$onists

/ +icotinicAcetylcholinerecetora$onists"other than$rou 9#

Sinosyns Sinosad

) Chloride

channelactivators

Aver%ectins A!a%ectin

; Co%oundsof unknownor nonsecific%ode ofaction"selective

feedin$ !lockers#

Cryolite Cryolite

(( Micro!ialdisrutors ofinsect %id$ut%e%!ranes

Bacillus

thuringiensis su!s&tenebrionisendotoinsBt

(/ 'nhi!itors ofchitin

!iosynthesis,tye 2,>eidoteran

Benzoylurea +ovaluron

(8 B Ecdysonea$onists L

%oultin$

Azadirachtin +ee%



disrutors

** olta$e-deendentsodiu%channel

!locker

'ndoacar! 'ndoacar!

*/ +euronalinhi!itors

"unknown%ode ofaction#

Bifenazate Bifenazate

+ot surrisin$ly, hi$h selection ressure eventually resulted in a lar$e nu%!er ofinsecticide-resistant Colorado otato !eetle oulations, with resistance raidly

ro$ressin$ since the %iddle of the last century "=i$& (#&



.i$h redisosition to resistance develo%ent is ro!a!ly caused !y a nu%!er offactors& =irst, lants in the fa%ily Solanaceae have hi$h concentrations of toic$lycoalkaloids in their folia$e& Therefore, coevolution of the !eetle and its host

lants re4uired develo%ent of the hysiolo$ical caa!ility to detoify or tolerate

oisons "=erro (;;@ Bisho and Grafius (;;)#& Secondly, hi$h !eetle fecundity !oth increases the ro!a!ility of rando% %utations, as well as ensures the raid !uild-u in nu%!ers of resistant %utants once such %utations have occurred"Bisho and Grafius (;;)#& Thirdly, the !eetles have a narrow host ran$e, and !othlarvae and adults feed on the sa%e host lants& This reduces the size of anunstructured refu$e where susceti!le $enotyes %ay escae eosure to che%icals"Bisho and Grafius (;;)@ <halon and =erro (;;8#& Althou$h so%e susceti!le

!eetles %ay survive on untreated volunteer otatoes within fields rotated toalternate cros or on solanaceous weeds, their nu%!er is aarently insufficient forreducin$ the fre4uency of resistant alleles !elow the econo%ically si$nificant level& =ourthly, with the ecetion of cro rotation, $rowers rely al%ost eclusively on



insecticides for !eetle control !ecause other control techni4ues do not rovide afeasi!le alternative ".arcourt (;?(@ Casa$rande (;8?@ Bisho and Grafius (;;)#&This increases selection ressure towards resistance& =inally, !ein$ native to +orthA%erica, the Colorado otato !eetle did not under$o $enetic !ottleneck tyical ofintroduced ests ".awthorne *22(@ <e!er *22#& Such $enetic varia!ility %ay

rovide evolutionary lasticity necessary for adatation to adverse conditions&.owever, the relative i%ortance of the last factor is unclear !ecause resistance isalso a ro!le% in Euroe, where the Colorado otato !eetle is an introduced secies"<e!er *22#&

The first instance of Colorado otato !eetle resistance to synthetic or$anic esticides was noted for DDT in (;/* "Huinton (;//#& 1esistance to dieldrin wasreorted in (;/8, followed !y resistance to other chlorinated hydrocar!ons".of%aster et al& (;)?#& 'n su!se4uent years, failures have !een reorted for %ost

%a0or classes of insecticides "Ta!le *#& Althou$h the northeastern 7nited States isone of the %ain ro!le% areas "=or$ash (;8/@

Table 2. Insecticides to which the Colorado potato beetle has developed resistance as a result of

field e;posure or laborator9 selection #<halon et al. 200.

Chemical (roup Trade names

Car!a%ates Aldicar!, car!aryl, car!ofuran, cloethocar!,dioacar!, oa%yl, roour

5r$anohoshates Aza%ethihos, azinhosethyl,azinhos%ethyl, chlorfenvinhos,%alathion, %etha%idohos, %ethidathion,%onocrotohos, arathion, arathion-

%ethyl, horate, hos%et, hoi%,4uinalhos, tetrachlorvinhos, trichlorfon

5r$anochlorines DDT, %ethoychlor

Cyclodiene 5r$anochlorines Aldrin, chlordane, dieldrin, endosulfan,endrin, .C.-$a%%a, toahene



5r$anotins Azocyclotin

'nor$anics .ydro$en cyanide

yrethroids, yrethrins Cyer%ethrin, delta%ethrin, esfenvalerate,fenvalerate, er%ethrin

'soflavones 1otenone

+eonicotinoids thia%ethoa%, aceta%irid, clothianidin,dinotefuran, i%idaclorid, +-des%ethylthia%ethoa%, +-%ethyli%idacloridnitenyra%, thiaclorid

Macrocyclic lactones "aver%ectins# A!a%ectin

+ereistoin analo$ues Carta

Sinosyns Sinosad

Bacillus

thuringiensissu!s& tenebrionisendotoinsBt

<halon and =erro (;;8#, insecticide resistance in the Colorado otato !eetle is atruly $lo!al heno%enon ".of%aster et al& (;)?@ =or$ash (;8/@ Boiteau (;88!@'oannidis et al& (;;(@ .ei% et al& (;;*@ Stewart et al& (;;?@ +oronha et al& *22(@Stankovic et al& *229@ our%irza *22/@ Mota-Sanchez et al& *22)@ Benkovskaya etal& *22)@ Moha%%adi Sharif et al& *22?@ <halon et al& *228#& 5!viously, not every

!eetle oulation is resistant to every sin$le co%ound that has ever !een o!servedto fail a$ainst this est& .owever, !oth cross-resistance and %ultile resistanceaear to !e very co%%on within the tested oulations ".arris and Svec (;8(@'oannidis et al& (;;(@ .ei% et al& (;;*@ Stewart et al& (;;?@ Mota-Sanchez et al&

*22)@ Alyokhin et al& *22), *22?@ <halon et al& *228#&1esistance ro!le%s reached critical levels in the 7&S& in the early (;;2s, when



$rowers in so%e otato-roducin$ re$ions co%letely ran out of che%ical controlotions& Arrival of neonicotinoid insecticides in (;;/ !rou$ht a eriod of relief inareas where the !eetles had develoed resistance to other che%icals "<halon and=erro (;;8#& .owever, the first instances of resistance to i%idaclorid were soonreorted fro% co%%ercial otato far%s in several 7&S& states "hao et al& *222@5lson et al& *222@ Mota-Sanchez et al& *22)@ Alyokhin et al& *22), *22?#& <hile anu%!er of new che%istries are eected to aear on the %arket in the near future,there is no reason to !elieve that any of the% will !reak the see%in$ly endlessinsecticide resistance new insecticide cycle that is so characteristic of theColorado otato !eetle %ana$e%ent "=i$& *#&

'nsecticide resistance is likely to !e a serious ro!le% even when alternativeche%istries are availa!le to control resistant !eetles& =irst, develo%ent of newinsecticides is increasin$ly eensive, which affects their %arket rice aid !y$rowers& Grafius "(;;?# conducted an etensive four-year study of the econo%ici%act of the Colorado otato !eetle insecticide resistance on the Michi$an otatoindustry& The esti%ated lon$-ter% increased cost ran$ed fro% N99 to N);Lha, withoverall state-wide losses addin$ u to as %uch as N(&9 %illion er year& Secondly,



availa!le alternatives %ay !e less convenient and %ore environ%entally da%a$in$than the failed insecticides they have to relace& =or ea%le, i%idaclorid !eca%eineffective for controllin$ Colorado otato !eetles on two co%%ercial far%s inSouthern Maine "Alyokhin et al& *22?#& As a result, the $rowers were forced torelace a sin$le alication of i%idaclorid in-furrow at lantin$ with %ultilefoliar alications of oa%yl and a!a%ectin& Both co%ounds have hi$her%a%%alian toicity than i%idaclorid, and foliar srays increase worker eosureand the ossi!ility of drift& Third, a threat of insecticide failure due to resistancedevelo%ent increases the already hi$h real and erceived risks of otato far%in$&

R3IT!&C3 !!7 83T61D

'n the field, insecticide resistance can !e o!served as little or no reduction in thedensity of !eetle oulations and their da%a$e to otato lants followin$insecticide alication "assu%in$ that other ossi!le reasons, such as oor ti%in$ or %alfunctionin$ sray e4ui%ent, could !e ruled out#& 'n the la!oratory, resistancecan !e %easured as an increase in the dose ">D/2# or concentration ">C/2# of thetoin re4uired to kill /2 of the eosed oulation& >D/2 values are used whenthe eact dose received !y each tested insect is known "e&$&, when a drolet of theknown volu%e of the known concentration of insecticide solution is aliedtoically to an insect#& >C/2 values are used when the eact dose is not known

"e&$&, when an insect feeds on the leaf treated with the known concentration ofinsecticide solution, !ut the eact a%ount of in$ested %aterial is not %easured#&Bioassays nor%ally consist of rearin$ serial dilutions of tested che%icals andthen alyin$ the% to !eetles ori$inatin$ fro% oulations of interest& >D/2 or>C/2 values are then deter%ined usin$ ro!it analysis& 1esistance ratios are oftencalculated as the ratio of >D/2 or >C/2 value o!tained for a resistant oulation tothe >D/2 or >C/2 value o!tained for a control oulation that is known to !esusceti!le to the tested che%ical& Discri%inatin$ doses or concentrations "e&$&, theconcentration that kills O/ of !eetles fro% resistant oulations !ut P;2 ofsusceti!le !eetles# can also !e deter%ined fro% la!oratory !ioassays for 4uickidentification of resistant !eetles ".ei% et al& (;;2@ Bisho and Grafius (;;(#&

Because differences in susceti!ility to insecticides %ay !e considera!le a%on$Colorado otato !eetle life sta$es, >D/2 or >C/2 values and resistance ratios %aydiffer deendin$ on which life sta$e was assessed "Silco et al& (;8/@ ehnder(;8)@ ehnder and Gelernter (;8;@ <ieren$a et al (;;)@ hao et al& *222#& =orea%le, i%idaclorid resistance ratios differed !y al%ost an order of %a$nitudewhen %easured in *nd instar larvae co%ared to adults "hao et al& *222#& As aresult, susceti!ility studies erfor%ed for one life sta$e %ay not accurately reflect

susceti!ility at a oulation level "our%irza *22/#, nor do they necessarilyaccurately redict insecticide erfor%ance in the field&



Different studies rely on different eosure %ethods in their !ioassays& =orea%le, Boiteau et al& "(;8?#, Ar$entine et al& "(;8;a#, 'oannidis et al& "(;;(#,hao et al& "*222#, and Mota-Sanchez et al& "*22)# alied solutions of technical$rade insecticides in acetone toically to adult a!do%ens& Ar$entine et al& "(;8;a#also alied si%ilar solutions to the third dorsal a!do%inal se$%ent of fourthinstars, while Baker et al& "*22?# to the a!do%ens of early second instars& .ei%et al& "(;;2# and our%irza "*22/# laced first instars on aer disks treated withsolutions of co%%ercial insecticide for%ulations in acetone& Bisho and Grafius"(;;(# and Mowry and Sandvol "(;;/# laced adults on aer disks treated withsolutions of co%%ercial insecticide for%ulations in distilled water& <halon et al&"(;;# fed early second instars on insecticide-treated otato folia$e& 5lson et al&"*222# fed first instars on artificial diets %ied with serial dilutions of testedche%icals& .arris and Svec "(;8(# and Alyokhin et al& "*22)# alied co%%ercialinsecticide for%ulations to otted otato lants $rown in $reenhouses& our%irza

"*22/# died adults in water solutions of co%%ercial hosalone concentration or laced the% in $lass 0ars coated with acetone solutions of the sa%e co%ound&Mota-Sanchez et al& "*22)# in0ected solutions of technical $rade i%idaclorid indi%ethyl sulfoide throu$h the %e%!rane that connects second and third adulta!do%inal se$%ents& ariation in assay %ethodolo$y often co%licates theco%ara!ility of different studies, and so%e standardization would ro!a!ly !ehelful& .owever, it is to a certain de$ree unavoida!le !ecause of the diversity of

roerties and %odes of action of different insecticides and differin$ o!0ectives ofresearch&

't is i%ortant to realize that nu%erical increase in >D/2 or >C/2 values does notalways %ean noticea!le decline in insecticide efficiency in the field& =or ea%le,an increase of (/ to *2-fold in >D/2 in la!oratory assays was resent !eforereduced control with neonicotinoid insecticides was noticed in the field inMichi$an "Grafius unu!lished#& =irst, la!el alication rates are usuallyconservative enou$h to kill all !ut hi$hly resistant individuals& Secondly, dataresultin$ fro% !ioassays are usually hi$hly varia!le, and outliers %ay inflate the%eans& +evertheless, la!oratory investi$ations rovide valua!le insi$ht intoresistance status of oulations in 4uestion& Several studies directly confir%ed

su!0ective $rower assess%ent of oor insecticide erfor%ance in their fields !y theresults of la!oratory !ioassays "Boiteau et al& (;8?@ Stewart et al& (;;?@ Alyokhin etal& *22?#& Also, !ioassays %ay detect early shifts in resistance levels !eforefre4uency of resistant !eetles in a $iven oulation !eco%es aarent in the field&

P63&1T7PIC C6!R!CT3RITIC 15 R3IT!&T B33T3

ariation in assay %ethodolo$y often co%licates the co%ara!ility of different

studies, and so%e standardization would ro!a!ly !e helful& 1esistance levelsvary $reatly a%on$ different oulations "=or$ash (;8/@ Boiteau et al& (;8?@



Mowry and Sandvol (;;/@ Stewart et al& (;;?@ 5lson et al& *222# and !etween !eetle life sta$es "Silco et al& (;8/@ ehnder (;8)@ ehnder and Gelernter (;8;@our%irza *22/#, !ut in so%e cases could !e very hi$h& =or ea%le, .arris andSvec "(;8(# detected %ore than (,)22-fold increase in the >D/2 of car!ofuran inthe field oulation fro% Hue!ec& Si%ilarly, 'oannidis et al& "(;;(# o!served %orethan *,222-fold decrease in susceti!ility to car!ofuran and %ore than (,222-folddecrease in susceti!ility to azinhos%ethyl in so%e Michi$an oulations& Suchnu%!ers definitely indicate a considera!le resistance ro!le%& .owever, hi$hresistance ratios are not re4uired to identify a oulation as resistant& =or instance,a field oulation that could no lon$er !e controlled !y i%idaclorid in the study !yAlyokhin et al& "*22?# showed only 2-fold increase in >C/2 !ased on the resultsof larval la!oratory !ioassays& +u%eric outco%es of !ioassays are very deendenton the %ethodolo$y "our%irza *22/#, and their a!solute values should !einterreted with so%e caution& All in all, there is no dou!t that so%e Colorado

otato !eetle oulations are caa!le of develoin$ very hi$h levels of insecticideresistance&

'n addition to their a!ility to withstand insecticides, resistant !eetles %ay differfro% their susceti!le consecifics in other ways& Because of leiotroic effects ofresistant alleles, insecticide-resistant insects usually have reduced relative fitness inthe a!sence of insecticides "Crow (;/?#& The Colorado otato !eetle is noecetion& Beetles resistant to a variety of che%icals have !een shown to lay fewer e$$s, have lower rates of e$$ hatch, and develo %ore slowly co%ared tosusceti!le !eetles "Ar$entine et al& (;8;!@ Trisyono and <halon (;;?@ Alyokhin

and =erro (;;;c@ Baker et al& *22?#& Alyokhin and =erro "(;;;c# reorted thatoverwinterin$ %ortality was twice as hi$h for the !eetles resistant to Bacillus

thuringiensissu!s& tenebrionis CryA delta-endotoin "Bt# as for the susceti!le !eetles& Also, Baker and orter "*228# saw a si$nificant dro in i%idacloridresistance followin$ winter diaause, su$$estin$ lower survival of resistantindividuals& Alyokhin et al& "*22)# recorded increased %ortality of the first instarsin a different i%idaclorid-resistant oulation& Alyokhin and =erro "(;;;c#o!served a 92 dro in the nu%!er of coulations secured !y Bt-resistant %alesco%etin$ for the sa%e fe%ales with susceti!le %ales, !ut there was no difference

in fertilization success or coulation fre4uency on untreated folia$e !etweeni%idaclorid-resistant and i%idaclorid-susceti!le !eetles "Baker et al& *228#& =li$ht activity of Bt-resistant !eetles fed on untreated non-trans$enic folia$e wasnota!ly reduced co%ared to susceti!le !eetles "Alyokhin and =erro (;;;d#, andso was the srintin$ seed of i%idaclorid-resistant !eetles "Baker et al& *22?#&So%e of the resistance costs aear to !e ersistent, !ut others %i$ht decline overti%e, resu%a!ly due to allelic su!stitution or addition of %odifiers "Baker et al&*22?#&

Another reason why resistant oulations %i$ht differ henotyically fro%

susceti!le oulations is $enetic !ottleneck& 'nsecticide alications %ayeli%inate susceti!le $enotyes, thus reducin$ $enetic varia!ility of the survivin$



oulation& 1esistant founders %ay ossess rando% characteristics that are$enetically deter%ined, !ut not directly influenced !y resistant alleles& =orea%le, Benkovskaya et al& "*22)# o!served a %uch hi$her fre4uency of

henotyes with certain sot atterns on their heads, ronota, and elytra in the oulations of insecticide-resistant !eetles co%ared to the oulations ofsusceti!le !eetles& An overall diversity of sot atterns decreased over the ten-year eriod, resu%a!ly due to insecticide selection ressure& 'n!reedin$deression %ay also contri!ute to the decreased relative fitness of resistant insects,althou$h %ost studies also use hi$hly in!red la!oratory strains as susceti!lecontrols&

83C6!&I8 15 R3IT!&C3

3nown %echanis%s of Colorado otato !eetle resistance to insecticides includeenhanced %eta!olis% involvin$ esterases, car!oylesterases and %onooi$enases,tar$et site insensitivity, as well as reduced insecticide enetration and increasedecretion "1ose and Brindley (;8/@ Ar$entine et al& (;8;a@ 'oannidis et al& (;;(@'oannidis et al& (;;*@ <ieren$a and .ollin$worth (;;9@ Ansau$h et al& (;;/@ huet al& (;;)@ >ee and Clark (;;8@ Clark et al& *22(#& There is also so%e evidence of

!ehavioral resistance ".oy and .ead (;;/@ Alyokhin and =erro (;;;d#& 1esistance%echanis%s %ay !e hi$hly diverse even within a relatively narrow $eo$rahicalarea "'oannidis et al& (;;(#&

Cytochro%e 9/2 is involved in the %eta!olis% of internal hor%ones and liids ininsects, and also articiates in the %eta!olis% of eno!iotic co%ounds such as

esticides "=eyereisen *22/#& 'n the Colorado otato !eetle, the 9/2 deendent%onooy$enase syste% is the %ost co%%on %echanis% of resistance across %any

oulations fro% diverse $eo$rahical ori$ins&

'n vivo, re-treat%ent !y an oy$enase inhi!itor ieronyl !utoide "B5# reducedresistance of adult !eetles resistant to azinhos%ethyl "Aha%%ad-Sahi! et al&(;;9#, car!ofuran and car!aryl "1ose and Brindley (;8/#, fenvalerate "Soderlund et

al& (;8@ Silco et al& (;8/@ .arris and Turn!ull (;8)#, er%ethrin "Silco et al&(;8/#, and in 9th instar larvae reduce the resistance to a!a%ectin "oon et al&*22*#& Si%ilarly, i%idaclorid-resistant !eetles fro% >on$ 'sland, +ew orkshowed a reduction in resistance fro% 22-fold without B5 treat%ent to (28-foldwith B5 treat%ent "Mota-Sanchez et al& *22)#& The insect %eta!olis% ofi%idaclorid leads to the roduction of an olefin %eta!olite that is less toic to theinsect than the arent co%ound "Mota-Sanchez *22#& This heno%enon has !eeno!served in !oth susceti!le and resistant strains, !ut to a $reater etent in theresistance strains&



'n vitro, incu!ation of different su!strates with %icroso%es confir%ed thatresistance due to %onooy$enase activity was resent in resistant strains fro%>on$ 'sland, +ew ork and Michi$an "Aha%%ad-Sahi! et al& (;;9#&Monooy$enase activity was o!served in a variety of different su!strates includin$oidation of +AD., 5-de%ethylation, of -nitrianisole, +-de%ethylation ofa%inoyrine and eoidation of aldrin& A key findin$ was that %onooy$enaseactivity a$ainst a%inoyrine was lar$ely confined to the %icroso%al fraction ofho%o$enates and was %ore active in the larval $ut than in the fat !ody& Beetlestrain resistant to azinhos %ethyl also ehi!ited 9-fold hi$her %eta!olis% of thesu!strates ethoyresorufin and entoyresorufin "<ieren$a and .ollin$worth(;;9#& 'ncreased %eta!olis% and %icroso%al 9/2 levels were associated withresistance of 9th instar larvae to a!a%ectin "Goua%ene->a%ine et al& *22#& re-treat%ent with B5 suressed %eta!olis% of (9C-i%idaclorid in resistant

!eetles, rovidin$ further evidence of the role of B5 in suression of 9/2

%eta!olis% "Mota-Sanchez, unu!lished data#& Si%ilarly, the %ain %echanis%s ofresistance to azinhos%ethyl and er%ethrin have !een identified as increased%onooy$enase and arylesterase activity a$ainst azinhos %ethyl and er%ethrin"Ar$entine et al& (;8;a#& Enhanced car!oylesterase activity also contri!uted to

!eetle resistance to er%ethrin "Ar$entine et al& (;;/@ >ee and Clark (;;)#& 'naddition, $luthione-S-transferase activity was elevated in the >on$ 'sland strainresistant to azinhos%ethyl, as well as in the Michi$an strain resistant toazinhos%ethyl, er%ethrin and car!ofuran "Aha%%ad-Sahi! et al& (;;9#&

Tar$et site insensitivity is another i%ortant %echanis% of !eetle resistance to

insecticides& Altered acetylcholine esterase lays a critical role in resistance toor$anohoshates and car!a%ates "'oannidis et al& (;;*@ <ieren$a and.ollin$worth (;;@ Stankovic et al& *229#& Beetles resistant to azinhos%ethylcontained two %utations in the AChE "S*;(G and 123#, which %ade the enzy%eless sensitive to azinhos%ethyl and car!ofuran "3i% and Clark *22*@ 3i% et al&*22)#& 'n the strain resistant to car!ofuran, the resence of two %utations "';*Tand S*;(G# did not result in resistance, !ut the resence of 0ust one "S*;(G#conferred hi$h resistance to car!ofuran and %ediu% resistance to azinhos%ethyl"3i% et al& *22?#& A strain resistant to azinhos%ethyl !ecause of an altered

acetylcholine esterase had a reduced su!strate affinity for acetylthiocholine andazinhos%ethyl oon in co%arison with a susceti!le strain "Clark (;;?#&

1esistance due to the chan$es in acetylcholine esterase %ay !e selective& =orinstance, <ieren$a and .ollin$worth "(;;# found that while one resistant strainwas hi$hly insensitive to arylcar!a%ates, another strain with the sa%e affectedenzy%e was hi$hly insensitive to or$anohoshates, !ut not arylcar%a!ates&'nterestin$ly, acetylcholinesterase alteration %ade yet another resistant strain %oresensitive to Q-chaconine, a $lycoalkaloid resent in otatoes and an inhi!itor ofacetylcholine esterase "<ieren$a and .ollin$worth (;;*#& 'n addition, altered

acetylcholine esterase also increased sensitivity to to%atine, a $lycoalkaloid foundin to%atoes "<ieren$a and .ollin$worth (;;*#&



Tar$et site chan$es are not li%ited to acetylcholine esterase& 'n a er%ethrin-resistant Colorado otato !eetle strain, a sin$le !ase air %utation "C to T# resultedin an a%ino acid chan$e "leucine to henylalanine, >(2(9=# in an Q-su!unit of thesodiu% channel& That %utation was the %a0or factor resonsi!le for nerveinsensitivity in Colorado otato !eetles when eosed to er%ethrin ">ee et al&(;;;, 3i% et al& *22/#& Also, nerve recordin$ su$$ested that insensitivity at thetar$et site %ay !e one of the %echanis%s of !eetle resistance to i%idaclorid "Tanet al& *22/#& .owever, althou$h %utation in the nicotinic acetylcholine recetorwas resonsi!le for resistance of the !rown lanthoer to i%idaclorid ">iu et al&*22)#, no %utation has !een reorted in the alha su!units of the tar$et siteresonsi!le for resistance in the Colorado otato !eetle& Additionally, nodifferences were found in !indin$ recetors of .-i%idaclorid in resistant andsusceti!le !eetles "+auen and Denhol% *22/#&

1educed enetration and increased ecretion aear to !e less i%ortant inreducin$ Colorado otato !eetle sensitivity to insecticides& +evertheless, they alsohave their role to lay& Ar$entine et al& "(;;9# found that these %echanis%s %ayact to$ether with enhanced %eta!olis% and tar$et site insensitivity to reducetoicity of azinhos%ethyl& 1educed enetration and increased ecretion were alsoi%ortant in car!aryl resistant !eetles "1ose and Brindley (;8/#& 'n addition, raidecretion has !een identified as a %echanis% to re%ove i%idaclorid "Mota-Sanchez *22# and $lycoalkaloids "3rishnan et al& *22?# fro% the insect !ody& Invivodistri!ution and %eta!olis% studies usin$ R(9C i%idaclorid su$$ested thatthe tolerance o!served in a resistant oulation fro% >on$ 'sland, +ew ork was

ri%arily due to increased ecretion of the arent co%ound "5lson *222#&

Behavioral resistance has !een studied in the Colorado otato !eetles resistant toBt& Alyokhin and =erro "(;;;d# reorted that the in$estion of the toinsi$nificantly increased fli$ht activity in the resistant strain, su$$estin$ that

hysiolo$ical resistance was ro!a!ly reinforced !y the !ehavioral escae fro% thetoic environ%ent& Such a resonse was dislayed !oth !y !eetles continuouslyfed on trans$enic lants and !y !eetles fed on re$ular lants !efore feedin$ ontrans$enic lants& A si%ilar effect was reorted !y .oy and .ead "(;;/#, who

o!served that Colorado otato !eetle larvae with hi$her hysiolo$ical resistance toBt co%ared to susceti!le larvae were also %ore !ehaviorally resonsive, %ovin$away fro% the folia$e treated with the hi$her toin concentrations&

:3&3TIC 15 R3IT!&C3

Genetic analyses of resistance in the Colorado otato !eetle have !een carried outon car!a%ates, or$anohoshates, yrethroids, Bacillus

thuringiensis su!s& tenebrionis delta-endotoin, and neonicotinoids& There have !een four !asic desi$ns used to elucidate the $enetics of insecticide resistance,



often in co%!ination& A ositive resonse to selection can show in the si%lestsense the resence of additive $enetic variance for resistance "Ar$entine and Clark(;;2@ 'oannidis et al& (;;*@ <halon et al& (;;@ 1ahard0a and <halon (;;/@Trisyono and <halon (;;?@ Miyo et al& (;;;#& Crosses !etween resistant andsusceti!le strains with !ackcrosses of hy!rids to susceti!les have !een used to%easure do%inance, se linka$e and sin$le-locus vs& oly$enic deter%ination ofresistance "Ar$entine et al&(;8;a@ .ei% et al& (;;*@ 'oannidis et al& (;;*@ 1ahard0aand <halon (;;/@ Baker et al& *22?#& Huantitative $enetic esti%ates of herita!ilityhave !een used to show otential for su!se4uent resistance evolution ".oy and.ead (;;/@ Miyo et al& (;;;@ Baker et al& *22?#& =inally, linka$e %ain$".awthorne *22# and cD+A se4uencin$ "hu and Clark (;;/# have !een used toidentify secific $enes associated with resistance&

Several factors ose challen$es for $enetic analyses of resistance& The different

assay techni4ues descri!ed a!ove ose challen$es in ter%s of validity andrelia!ility& Direct alication of a dissolved technical roduct is the least varia!leand %ost reeata!le %ode of alication, !ut %ay not act in the sa%e way as anin$ested toin& esticides can have very different effects on different a$e classes"see a!ove#& arent-offsrin$ re$ression, one of the si%lest %ethods of %easurin$additive $enetic variation, is not availa!le in its usual for%, !ecause scorin$ thetrait usually involves %ortality& <hile an assay is usually 4ualitative, re$isterin$survival or %ortality, the trait of interest is 4uantitative, i&e&, ro!a!ility of death&The 4uantitative $enetic analysis of threshold traits such as se-ratio of offsrin$"Bul%er and Bull (;8*# can !e alied to analysis of resistance, thou$h there is still

difficulty in usin$ an assay that %i$ht kill off the arentals of a su!se4uent$eneration& 5ne way of dealin$ with this is to use the >D/2 of entire fa%ilies as a%easure of resistance, and co%are resistance of offsrin$ with $randchildren,usin$ >D/2 of full si!lin$ fa%ilies as a roy for arental resistance "Baker et al&*22?#& A half-si! desi$n, where several %ales are %ated to at least two fe%aleseach and the variance within da%s is co%ared to that a%on$ sires, can avoid so%eof these challen$es to deter%inin$ the herita!ility of resistance "3earsey and ooni(;;)#& =inally, costs of resistance can reduce $enetic variation for resistance fro%one $eneration to the net, and reduce the effectiveness of arent offsrin$

re$ression& This is seen %ost clearly in resistance $enes with hi$h associatedfitness costs, such as i%idaclorid "Baker et al& *22?#&

>a!oratory selection is eected to act differently than selection in the field& Thestron$ selection eerted !y hi$hly toic insecticides in the field is eected to favor do%inant, sin$le locus %utations conferrin$ resistance, while the weaker selection

ossi!le with the relatively s%all oulations sustaina!le in la!oratory eeri%entswill reveal s%aller additive effects fro% eistin$ $enetic variation "Mc3enzie*222#& .owever, !oth la!oratory selection eeri%ents and crosses usin$ fieldcollections have !een carried out usin$ the sa%e che%icals and those redictions

have not $enerally !een %et "Ta!le #& =or ea%le, car!ofuran resistance wasea%ined $enetically twice, once usin$ la!oratory selection "followin$ selection in



the field@ 'oannidis et al& (;;*# and once usin$ crosses fro% a field-resistant oulation ".ei% et al& (;;*#& The la!oratory selected oulation had a hi$herresistance ratio, %ore do%inant eression, and a closer %atch to sin$le-locus

redicted %ortality in the !ackcross& 'n fact, the two studies with the hi$hestde$ree of do%inance were la!oratory selection studies "'oannidis et al& (;;*@1ahard0a and <halon (;;/#& 1esistance was never recessive, and the overallavera$e value of D "after Stone (;)8@ where -( is urely recessive, 2 is urelyadditive, and ( is urely do%inant# in the studies analyzed was "MSD# 2&*(2&*;,reflectin$ sli$ht artial do%inance& Most studies found evidence of %ore than onelocus contri!utin$ to resistance, includin$ all studies usin$ field-resistant

oulations "Ta!le #&

Table ). ! summar9 of results of both selection e;periments and crosses amon( resistant and

susceptible lines.

Treatment :enerations oci e;-

lin/ed

Resistance

Ratio

Dominance% ource

Car!ofuran 9 ( +o /?) 2&)* 'oannidiset al&

(;;*

Car!ofuran Direct cross P( +o ); 2&*) .ei% etal& (;;*

Azinhos%ethyl Direct cross P( +o 9/ 2&*) Ar$entineet al&(;8;a

er%ethrin Direct cross P( es // 1ecessive Ar$entineet al&(;8;a

Esfenvalerate Direct cross ( or P(

es *2-*( Se%i-recessive

.ei% etal& (;;*



Esfenvalerate 9 P( es (8 -2&*) Miyo etal& (;;;

er%ethrin Direct cross n&a& es 9(-9?&/ Se%i-recessive

=ollett etal& (;;

'%idaclorid Direct cross P( +o (22&8 or (&*

-2&* or -2&(2)

hou etal& *222

'%idaclorid (, P( +o )&)-*(&89

2&(/-2&(8 Baker etal& *22?

Btt *; P( +o *; 2&?? <halon etal& (;;,1ahard0aand<halon(;;/

A!a%ectin ? n&a& +o (/-* 2&*; Ar$entineand Clark(;;2

A!a%ectin ?, )* n&a& +o (/-* 2&*;, 2&(; Ar$entineand Clark

(;;2

( Either the nu%!er of $enerations of selection if selection was carried out rior tocrossin$, or UDirect crossJ to si$nify either i%%ediate crosses !etween and withinresistant and susceti!le oulations, or !ackcrossin$&* Two searate oulations were selected in this study& The lar$er ratio was o!served when resistance was assayed in adults, the s%allerin *nd-instar larvae&9 E The s%aller ratio was in *nd-instars in Massachusetts in (;;;, the hi$her ratio

was fro% a 1esistant field in Maine in *22/&/ Do%inance of the >D/2 or >C/2 was calculated as in Stone "(;)8#& 't ran$es



fro% -( "urely recessive# to ( "urely do%inant#, with 2 reflectin$ urely additiveinheritance& <hen not reorted it was calculated fro% the reorted 11, SS, and 1S>D/2Us, in the autoso%al cases, and descri!ed 4ualitatively "ecet in Miyo et al&(;;;# in se-linked characters&) The %ore recessive value was %easured in adults, the %ore additive one in larvae&

'%idaclorid has !een a recent focus of research, due to its heavy use !y the otatoindustry for control of Colorado otato !eetles since (;;/& <hile no $enetic%ain$ of i%idaclorid resistance has !een carried out, si%le crosses haveshown that resistance is autoso%al, with artially recessive or artially do%inantinheritance o!served in different studies "Ta!le #& Do%inance can evolve"Bour$uet et al& *222#, and the different values %easured could have a si$nificanteffect on resistance evolution, !ut it is not ossi!le to deter%ine the si$nificance ofdifferences !etween the earlier result lookin$ at a >on$ 'sland + oulation

"hao et al& *222# and later results fro% Massachusetts and Maine oulations"Baker et al& *22?#, !ecause the two studies looked at different a$e classes& Theearlier study ea%ined do%inance in adults "and found different values deendin$on the day of scorin$# and the later study looked at larval survival& Do%inant$enetic control is a challen$e for resistance %ana$e%ent !ecause it reservesresistant alleles found in hy!rid offsrin$, which is where %ost resistance allelesare found when resistance is rare& 5nce resistance is co%%on this is less of a

ro!le%, !ecause a s%aller roortion of resistance alleles are found inheterozy$otes& .owever, the $reater the do%inance of resistance, the hi$heralication rate will !e needed to control a $enetically hetero$enous oulation& 't

re%ains to !e seen how the $enetic underinnin$s of resistance in different$eo$rahical locations varies& Do%inance of fitness costs has a si$nificant effect onresistance evolution in evolutionary %odels "Carriere et al& *22/#& 7nfortunately,the only %easures thus far on do%inance of fitness costs found a fecundity cost to

!e recessive and a hatch ti%e cost to !e additive "Baker et al& *22?#&

1esistance to i%idaclorid is likely oly$enic& 'n two studies, o!served %ortalityof !ackcross ro$eny was si$nificantly different fro% redicted %ortality usin$ asin$le $ene %odel "hao et al& *222@ Baker et al& *22?#& Multile %echanis%s of

resistance, resu%a!ly under control of different loci, have !een indicated inseveral studies& Syner$is% studies "hao et al& *222@ 5lson *222@ Mota-Sanchez etal& *22)# have shown a artial role for %ied-function oydases, and a recetorsensitivity %echanis% has also !een descri!ed "Tan et al& *228#&

Huantitative $enetic analyses can add another di%ension to our understandin$ ofresistance evolution& Sloes of dose-resonse curves are li%ited in their a!ility to%easure relative and a!solute a%ounts of $enetic varia!ility for resistance"Mc3enzie *222#& .erita!ilities are valid only within the oulation %easured,thou$h different oulations can !e co%ared in a la!oratory settin$& They are also

snashots in ti%e, !ecause novel %utations can $enerate new $enetic variance&.owever, they are the !est %easure of current additive $enetic variance& There have



!een three esti%ates of herita!ility of resistance in the Colorado otato !eetle& Afull-si! desi$n reorted a herita!ility of 2&? for tolerance to B. thuringiensis delta-endotoin ".oy and .ead (;;/#& A half-si! desi$n reorted a herita!ility of 2&9/"!ut the value was not si$nificantly different fro% 2# for tolerance to esfenvalerate"Miyo et al& (;;;#& A study usin$ arent-offsrin$ re$ression reorted a herita!ilityof 2&8) for i%idaclorid tolerance "Baker et al& *22?#& .i$h variance in insecticideresistance syste%s is usually interreted as reflectin$ a otential to raidly losesusceti!ility& .owever, hi$h herita!ilities, and hi$h levels of additive variation,can also reflect oosin$ selection on resistance due to fitness costs of resistance,as each $eneration eeriences the oosin$ forces of selection due to insecticidealication and costs of resistance&

Molecular $enetic analyses of resistance have !een carried out on yrethroids andazinhos%ethyl, an or$anohoshate& The se linka$e and oly$enic effects on

er%ethrin resistance o!served in earlier studies was confir%ed usin$ HuantitativeTrait >ocus "HT># %ain$ ".awthorne *22#, and $enotyin$ tests for the locuswith the stron$est effect have !een develoed "3i% et al& *22/#& A %utationalchan$e in the acetylcholine recetor of azinhos%ethyl resistant otato !eetles wasse4uenced "hu and Clark (;;?#& Molecular $enetic studies should aid inidentifyin$ %echanis%s of resistance, and should also identify when individualresistance %utations are shared !y different oulations and contri!ute to resistancea$ainst different active in$redients&

R3IT!&C3 8!&!:383&T

1educin$ insecticidal ressure on est oulations is a co%%only roosedstrate$y to delay evolution of resistance "McGau$hey and <halon (;;*@ Ta!ashnik (;;9@ Cario (;;8, CarriVre and Ta!ashnik *22(#& Selection towards insecticideresistance could !e alleviated !y relacin$ at least so%e of the srays !y non-che%ical control techni4ues& Cro rotation for the Colorado otato !eetle controlhad !een first reco%%ended as early as (8?* "Bethune (8?*#, and since then

roved to !e a $ood control strate$y "Casa$rande (;8?#& At the rotated field, eakdensity of the !eetle e$$ %asses could !e /-(2 of that of the non-rotated field">asho%! and +$ (;89@ <ri$ht (;89#& 7nfortunately, hi$h !eetle %o!ilitynecessitates a considera!le searation !etween the rotated fields to %ai%izeefficiency of this techni4ue "<eisz et al& (;;9, (;;)@ .ou$h-Goldstein and <halen(;;)#& Still, cro rotation re%ains the sin$le %ost i%ortant cultural controla$ainst the Colorado otato !eetle& 5ther cultural ractices that show otential to reduce !eetle da%a$e include%aniulation of lantin$ ti%e "<e!er and =erro (;;9#, use of tra cros "<e!er

and =erro (;;9@ .oy et al& (;;)#, %ulches "ehnder and .ou$h-Goldstein (;;2@Stoner (;;@ Brust (;;9#, lastic-lined trenches alon$ field !orders "Misener et al&



(;;@ Boiteau et al& (;;9#, and destruction of overwinterin$ ha!itats "Milner et al&(;;*#& +atural ene%ies can also have a su!stantial ne$ative i%act on !eetle

oulations ".ou$h-Goldstein et al& (;;@ =erro (;;9#, !ut !ecause of the hi$hColorado otato !eetle fecundity they usually cannot suress !eetle oulations

!elow econo%ically da%a$in$ levels& Ecet for cro rotations, the overallfeasi!ility of alternative control techni4ues is usually not sufficient to allow theirlar$e-scale adotion in co%%ercial roduction&

.ost lant resistance is a otentially valua!le tool for %ana$in$ Colorado otato !eetles that could reduce the nu%!er of insecticide alications& 7nfortunately,resistant cultivars are not currently availa!le& Althou$h nu%erous Solanum s&have resistance to insects, otato !reedin$ is co%licated !y the otatoJs tetraloidyand these roerties have not !een transferred into co%%ercially desira!le cultivars"Grafius and Douches *228#& Genetically %odified otatoes eressin$ Bacillus

thuringiensis delta-endotoin that is toic to the Colorado otato !eetle werere$istered and sold in the 7&S& fro% (;;/*222, !ut were discontinued in resonseto consu%er concerns a!out $enetically %odified cros "Grafius and Douches*228#&

1otation !etween insecticides with different %odes of action is one of the %ostco%%only reco%%ended resistance %ana$e%ent techni4ues "'nsecticide1esistance Action Co%%ittee *228@ +ational otato Council *228#& This aroach%ay work articularly well when $rowers ractice inte$rated est %ana$e%ent andno insecticide alications are %ade unless !eetle densities eceed econo%ic

thresholds& 7nfortunately, Colorado otato !eetles are co%%only resistant to%ultile che%icals !elon$in$ to different insecticide classes and resistance%echanis%s %ay !e hi$hly diverse even within a relatively narrow $eo$rahicalarea "'oannidis et al& (;;(#& Also, there is a considera!le variation in toicity toColorado otato !eetles of different insecticides !elon$in$ to the sa%e che%icalclass "=or$ash (;8/@ Boiteau et al& (;8?@ Alyokhin et al& *22)@ Mota-Sanchez et al&*22)#& All this %akes selection of aroriate rotation che%icals a ratherchallen$in$ task& =urther%ore, !eetle oulations on %ost co%%ercial far%s havea lon$ history of eosure "and su!se4uent resistance# to a variety of che%ical

classes& Althou$h fre4uency of alleles conferrin$ resistance to a $iven insecticideis likely to decline after a $rower stos usin$ it, it will still stay elevated co%aredto uneosed oulations& As a result, there will likely !e reinvi$oration ofresistance develo%ent to at least so%e of the older che%icals followin$ their re-introduction to the rotation se4uence "Alyokhin et al& *22)#& 3nowin$ the astinsecticide eosure and current susceti!ility to individual insecticides for a

articular Colorado otato !eetle oulation is i%ortant for achievin$ $ood levelsof its suression& Si%le relace%ent of one class of che%icals with another isnot necessarily $oin$ to work&

Satial refu$es can !e created !y leavin$ a roortion of the field "usually a!out*2# untreated with insecticides to suort a oulation of susceti!le individuals



sufficient to curtail %atin$ !etween resistant individuals "<halon and =erro (;;8#&Success of this aroach deends on the eistence of a lar$e oulation ofsusceti!le individuals and a si$nificant $ene flow !etween resistant andsusceti!le Colorado otato !eetle oulations& Matin$ !etween resistant andsusceti!le !eetles is likely to !e encoura$ed !y hi$h !eetle %o!ility "eseciallywhen cro rotation is racticed# and an etended eriod of seual activitycharacteristic of this secies& <hen resent, !ehavioral avoidance of toicenviron%ents !y resistant !eetles %ay further increase an outflow of resistantalleles fro% the %ain cro into refu$es "Alyokhin and =erro (;;;d#, where aho%ozy$ously resistant oulation is unlikely to esta!lish !ecause of its reducedrelative fitness "Trisyono and <halon (;;?@ Alyokhin and =erro (;;;c#& Geneflow, and refu$e success, will !e li%ited !y differences in henolo$y in treated anduntreated areas& 'nco%lete resistance, leadin$ to lon$er develo%ent ti%e intrans$enic Bt cros has !een identified as an o!stacle to $ene flow and refu$e

success in the cotton est ink !ollwor% %oth, Pectinophora gossypiella ">iu et al&(;;;#& A si%ilar effect on henolo$y was seen in the Colorado otato !eetle

oulations on i%idaclorid treated and untreated sides of a sin$le field& 'n thatstudy the eak in lar$e "third or fourth instar# larval density was delayed !y 2 daysin the first su%%er $eneration "Baker et al& *22(#& 'f $ene flow durin$ the su%%er$enerations is ha%ered !y chan$es in henolo$y, the !ulk of $ene flow %ust take

lace in the oulations e%er$in$ fro% diaause in the srin$&

<hen !eetles a$$re$ate in overwinterin$ sites outside of the field "<e!er and =erro(;;#, this will also contri!ute to $ene flow !etween resistant and susceti!le

oulations& After diaause ter%ination, a si$nificant roortion of ost-diaause !eetles %ate within or near overwinterin$ sites "=erro et al& (;;;#& Sinceoverwinterin$ survivorshi %ay !e hi$her for susceti!le !eetles than for resistant

!eetles "Alyokhin and =erro (;;;c@ Baker and orter *228#, and susceti!le %ales%ay secure %ore er caita coulations than resistant %ales "Alyokhin and =erro(;;;c#, there is an increased ro!a!ility that a survivin$ ost-diaause resistantfe%ale will %ate in the srin$ with a susceti!le %ale& Ser% fro% the srin$%atin$ takes al%ost co%lete recedence over the ser% fro% the re-diaause%atin$ "Baker et al& *22/#& As a result, fre4uency of resistant ho%ozy$otes in ost-

diaause !eetle oulations would !e lower than in the oulations of su%%er-$eneration !eetles& 5rientin$ untreated areas arallel to overwinterin$ sites willencoura$e susceti!le !eetles fro% refu$es and resistant !eetles fro% the %ain croto overwinter in the sa%e sites "=erro et al& (;;;#&

1efu$es could !e created !y leavin$ !locks of untreated lants ad0acent to thetreated fields, !y leavin$ untreated stris within the lar$er fields "<halon and =erro(;;8#, or !y usin$ eri%eter srays or at-lantin$ treat%ents with a !lock ofuntreated rows in the %iddle of the field "Dively et al& (;;8@ Blo% et al& *22*#&Colonization of otato cros !y insect ests starts at field ed$es, and then

ro$resses towards the field center "oss and =erro (;;2@ <e!er and =erro (;;@Boiteau et al& (;;9@ Di=onzo et al& (;;)#& Therefore, eri%eter treat%ent rovides



rotection to the untreated refu$e !ecause treated rows serve as !arriers to the estscolonizin$ otato fields& .owever, leavin$ too narrow of a treated eri%eter %ayresult in inade4uate cro rotection "Blo% et al& *22*#& At the sa%e ti%e, too widea eri%eter %ay de-facto eli%inate the refu$e !ecause susceti!le colonizers erishwhile tryin$ to cross the treated areas&

Althou$h the idea of a satial refu$e is very oular in the acade%ic co%%unity,%ost co%%ercial $rowers erceive this aroach as risky and are reluctant toi%le%ent it on their far%s !ecause of the hi$h value of the otato cro and thedifficulty often encountered controllin$ Colorado otato !eetles& Delayin$resistance develo%ent is a so%ewhat a!stract and distant !enefit, while reducedyield due to !eetle da%a$e is a real and resent loss& <hen leavin$ a refu$e is ale$al re4uire%ent, as is the case with trans$enic corn and cotton lants eressin$Bt-toins in their folia$e, the $rowers nor%ally insist on treatin$ it with che%icals

that have a different %ode of action& Deendin$ on the che%icals used and thefre4uency of their alication, this %ay effectively cancel the refu$e !y killin$%ost "if not all# of its inha!itants&

't is hi$hly unlikely that there is a silver-!ullet solution to the ro!le% ofinsecticide resistance in the Colorado otato !eetle& By itself, none of the discussedtechni4ues will !e successful in reservin$ efficiency of cro rotection che%icals&1esistance develo%ent is a dyna%ic evolutionary rocess that could !e likened toan ar%s race !etween hu%ans co%in$ u with new toins and ways of theirdeloy%ent and ests develoin$ new adatations "Denhol% and 1owland (;;*#&

5nly a truly inte$rated aroach to est %ana$e%ent will ensure lon$-ter% successin che%ical est control "which is another way of sayin$ Wwill revent resistancedevelo%entX#& To continue the %ilitary analo$y, the sa%e three !asic rincilesthat aly to any hostile encounter also aly to suression of the Colorado otato

!eetle oulations& =irst, it is essential to know and understand the ene%y&Secondly, it is necessary to use a %ultile attack strate$y& 1elyin$ on a sin$le tacticis usually doo%ed to failure, even if this tactic is sound in $eneral "0ust think of anar%y that consists eclusively of tank !ri$ades, without infantry, aviation, oren$ineerin$ cors#& Third, it is i%ortant to strike hard, !ut sto once the adversary

ceases hostilities and is ready to surrender&

'n ractical ter%s, an on-far% resistance %ana$e%ent lan should include thefollowin$ ele%ents6

(& Sule%entin$ insecticides with non-che%ical control %ethods "articularlycro rotations#&

*& Alternatin$ insecticides with different %odes of action&& 7sin$ econo%ic thresholds when %akin$ decisions a!out srayin$& Tryin$

to kill all the !eetles with insecticides usually results in killin$ all susceti!le

!eetles, while resistant !eetles survive and 4uickly !uild u their nu%!ers&



9& >eavin$ untreated refu$es for susceti!le !eetles& Econo%ic thresholdscannot !e used when insecticide is alied at lantin$ ti%e in furrow or as aseed treat%ent& Therefore, satial refu$es are re4uired to %aintain

oulations of susceti!le !eetles&/& 7sin$ full la!el rate of insecticides& Because resistance is usually

inco%letely do%inant, sufficiently hi$h dose of a toin will kill the !eetlesthat are heterozy$ous at the resistant allele&

)& Monitor for the si$ns of decreasin$ insecticide efficiency&

Si%ilar to other situations, an ounce of revention is likely to !e worth a ound ofcure when it co%es to resistance %ana$e%ent& 'n theory, reduced relative fitness of resistant !eetles should cause oulations to revert toward susceti!ility in thea!sence of selection ressure "Denhol% and 1owland (;;*#& 'ndeed, 1ahard0a and<halon "(;;/# reorted that under la!oratory conditions the ratio of Colorado

otato !eetle resistance to Bt decreased fro% *22 to 98-fold in (* $enerationswithout selection& .owever, it re%ained sta!le afterwards& The last $enerationtested in that study "(?th after re%oval of selection ressure# still was si$nificantly%ore resistant than unselected !eetles& Si%ilarly, !eetles on a co%%ercial far%re%ained tolerant to i%idaclorid for four years after the $rower discontinued usin$neonicotinoids "Alyokhin *22?#, desite the resistance-related reduction in relativefitness in that oulation "Baker et al& *22?#& 't is ossi!le that in the a!sence of arefu$e, susceti!le $enotyes are lar$ely eli%inated fro% the oulation& As aresult, the re%ainin$ $enetic variation is not sufficient to rovide a 4uick reversionto susceti!ility, even when susceti!le $enotyes have a hi$her relative fitness&

This stron$ly suorts takin$ a roactive aroach to resistance %ana$e%ent& 'twill !e too late to i%le%ent a %ana$e%ent lan after an insecticide has failed inthe field&

C4RR3&T !&D 54T4R3 C6!3&:3

'n his now classical treatise, Casa$rande "(;8?# descri!ed the lon$ history of theColorado otato !eetle control as W(/ years of %is%ana$e%ent&X The insecticideresistance crisis that was unfoldin$ at that ti%e was one of the ri%ary reasons forsuch an unflatterin$ definition, !ut the icture re%ains lar$ely the sa%e& Desiteall the scientific and technolo$ical advances, the Colorado otato !eetle continuesto !e a %a0or threat to otato roduction& 7nfortunately, there are co%ellin$reasons to !elieve that in the foreseea!le future, insecticide resistance in this insectwill re%ain a %a0or challen$e to the est control ractitioners&

=irst, our understandin$ of the Colorado otato !eetle !iolo$y is still inco%lete&'n so%e cases, reco%%endations on resistance %ana$e%ent are develoed !ased on

studies of as little as one resistant strain, often selected under la!oratoryconditions& Althou$h such an aroach is often valid, resistance %echanis%s %ay



!e diverse even within a relatively li%ited $eo$rahic area "'oannidis et al& (;;(#&Therefore, infor%ation o!tained in one location will not necessarily aly to otherlocations where resistance !eco%es a ro!le%& 'n other cases, reco%%endationsare %ade !ased on %athe%atic %odels, either secifically develoed for theColorado otato !eetleLotato syste% "=ollett et al& (;;, (;;/#, or !orrowed fro%other syste%s "e&$&, Baker et al& *22?#& A$ain, this could !e a valua!le aroach ifan aroriate %odel is selected& .owever, %odel assu%tions cannot !e taken for $ranted and should !e verified usin$ eeri%ental techni4ues& =or ea%le, haoet al& "*222# and Baker et al& "*22?# found evidence of oly$enic inheritance ofresistance to i%idaclorid in the field Colorado otato !eetle while %ost theoretical%odels advocatin$ hi$h dose refu$e aroach to insecticide resistance%ana$e%ent assu%e that resistance is controlled !y a sin$le $ene&

Secondly, so%e known asects of the Colorado otato !eetle life history co%licate

resistance %ana$e%ent& =or instance, a!out */ of recently e%er$ed su%%er$eneration !eetles stay close to the lace of their larval develo%ent until theirreroductive syste% is %ature "Alyokhin and =erro (;;;a#& Therefore, asi$nificant roortion of resistant !eetles develoin$ to adulthood on treated lantswill %ate with each other and leave ho%ozy$ously resistant offsrin$& Even whenresistant fe%ales reviously %ated to resistant %ales %ate to susceti!le %ales, uto half of their offsrin$ will still !e ho%ozy$ously resistant "Boiteau (;88a@Alyokhin and =erro (;;;!#& As a result, only co%lete cessation of %atin$

!etween resistant !eetles will re%ove all resistant ho%ozy$otes fro% the oulation& Clearly, that could hardly haen under field conditions&

.i$h Colorado otato !eetle %o!ility is also so%ewhat of a %ied !lessin$ when itco%es to resistance %ana$e%ent& 5n one hand, it encoura$es $ene flow !etweenrefu$es and the %ain treated cro& 5n the other hand, it %ay increase sread ofresistance a%on$ $eo$rahically isolated fields& Grafius "(;;/, (;;?# su$$estedthat unusually war% srin$ weather encoura$ed early !eetle e%er$ence fro%diaause in the srin$ of (;;( in Michi$an& Because !eetles were out of the soil

!efore e%er$ence of otato cro, %any of the% en$a$ed in lon$-distance %i$ratoryfli$ht in search of hosts& As a result, resistance !eca%e a ro!le% in reviously

unaffected areas, Colorado otato !eetle control costs rose !y half, and cro lossesto !eetle da%a$e went fro% virtually zero to as hi$h as (*&* "Grafius (;;?#&

Etended diaause is another life history trait otentially co%licatin$ resistance%ana$e%ent "<halon and =erro (;;8#& Efficiency of annual cro rotation forreducin$ field colonization !y overwinterin$ adults will o!viously !e di%inishedwhen a ortion of oulation re%ains dor%ant for two years& =urther%ore, it willco%licate insecticide rotations in a continuous otato cro& =or ea%le, so%e$rowers %ay want to alternate at-lantin$ alications of syste%ic neonicotinoidswith foliar alications of different che%icals durin$ the followin$ year& 'f

su!stantial nu%!ers of neonicotinoid-resistant !eetles do not eit their diaauseuntil the third year, efficiency of such an aroach is co%ro%ised& Even if the



field is rotated to a non-host cro in the third year, lon$-ter% disersal of resistant !eetles %ay eort resistance to other fields "Grafius (;;/#& Selection for%ultiyear diaause in resonse to cro rotation on co%%ercial far%s has !eenreorted for another leaf !eetle, northern corn rootwor% " Diabrotica barberi S%ithY >awrence# ">evine et al& (;;*#&

Third, revailin$ $rower attitude re%ains to !e a !arrier to wide-scale adotion ofresistance %ana$e%ent techni4ues& The 7S +ational otato Council has reco$nizedthe i%ortance of %ana$e%ent of resistance for the Colorado otato !eetle,diseases, and weeds, resultin$ in the develo%ent of educational %aterials thathave !een sent to $rowers throu$h state otato or$anizations "+ational otatoCouncil *228#& Althou$h there is a $eneral acknowled$e%ent of the ro!le%,dealin$ with it re%ains low on an avera$e $rowerJs list of riorities& =ew otatofar%ers are willin$ to %odify eistin$ ractices and suffer si$nificant

inconveniences or take on additional risks to delay Colorado otato !eetleadatation to insecticides& 'nstead, %ost of the% hoe that !y the ti%e when thecurrent che%ical of choice fails, the insecticide industry will co%e u with so%enew co%ound& A considera!le education effort on art of the research andetension co%%unity is re4uired !efore resistance %ana$e%ent !eco%es asessential a art of $ood esticide stewardshi as reventin$ drift or usin$ ersonal

rotection e4ui%ent&

5verco%in$ these challen$es is not an easy task& .owever, it is crucial forsustaina!le otato roduction& The era of a!undant and chea !road-sectru%

insecticides has co%e to an end& Develo%ent and re$istration of new insecticidesis an increasin$ly co%licated and costly rocess& At the sa%e ti%e, olderche%istries are !ein$ lost to resistance or re%oved fro% the %arket !ecause ofenviron%ental concerns& As a result, reservation of eistin$ roducts !eco%es a

ro$ressively %ore i%ortant task for every!ody involved in co%%erciala$riculture& 'nsecticide susceti!ility in est oulations should !e treated as avalua!le $enetic resource ".ueth and 1e$ev (;?9@ Bour$uet et al& *22/#, si%ilar todrou$ht tolerance or disease resistance in cultivated lants& Thus, its reservationneeds to !e taken etre%ely seriously !y all interested arties& Ecessive reliance

on che%icals is a dan$erous case of Wuttin$ all e$$s in one !asket,X with thefallacy of such an aroach !ein$ reeatedly and eensively de%onstratedthrou$hout the history of est control& 't is essential that for the years to co%e wehave a variety of techni4ues availa!le for suressin$ est oulations&

R353R3&C3 CIT3D



Aha%%ad-Sahi! 3', 1M .ollin$worth, ME <halon, M 'oannidis and E: Grafius&(;;9& olysu!strate %onooy$enases and other eno!iotic-%eta!olizin$ enzy%esin susceti!le and resistant Colorado otato !eetle& estic Bioche% hysiol 9;6(-(*&

Alyokhin A& *22?& 1esults of the *22? '%idaclorid resistance survey in Maine oulations of the Colorado otato !eetle& Sudlines 9/"#6-9&

Alyokhin A and D+ =erro& (;;;a& 1eroduction and disersal of su%%er-$eneration Colorado otato !eetle "Coleotera6 Chryso%elidae#& Environ Ento%ol*869*/-92&

Alyokhin A and D+ =erro& (;;;!& Electrohoretic confir%ation of ser% %iin$in %ated Colorado otato !eetles "Coleotera6 Chryso%elidae#& Ann Ento%ol Soc

A% ;*6*2-*/&

Alyokhin A and D+ =erro& (;;;c& 1elative fitness of Colorado otato !eetle"Coleotera6 Chryso%elidae# resistant and susceti!le to the Bacillus

thuringiensis CryA toin& : Econ Ento%ol ;*6/(2-/(/&

Alyokhin A and D+ =erro& (;;;d Modifications in fli$ht and oviosition of Bt-resistant and Bt-susceti!le Colorado otato !eetles as a result of eosureto Bacillus thuringiensis su!s& tenebrionisCryA toin& Ento%ol E Al ;26;-(2(&

Alyokhin A, G Dively, M atterson, D 1o$ers, M Mahoney and : <olla%& *22)&Susceti!ility of i%idaclorid-resistant Colorado otato !eetles to non-neonicotinoid insecticides in the la!oratory and field trials& A% : otato 1es 8698/-9;9&

Alyokhin A, G Dively, M atterson, C Castaldo, D 1o$ers, M Mahoney and :<olla%& *22?& 1esistance and cross-resistance to i%idaclorid and thia%ethoa%in the Colorado otato !eetle& est Mana$e Sci )6*-9(&

Ansau$h D, DG G 3ennedy and 1M 1oe& (;;/& urification and characterizationof a resistance-associated esterase fro% the Colorado otato Beetle, Leptinotarsa-

Decemlineata "Say#& estic Bioche% and hysiol /689-;)&

Ar$entine :A and :M Clark& (;;2& Selection for a!a%ectin resistance in Colorado otato !eetle "Coleotera, Chryso%elidae#& estic Sci *86 (?-*9&

Ar$entine :A, :M Clark and D+ =erro& (;8;a& Genetics and syner$is% ofresistance to azinhos%ethyl and er%ethrin in the Colorado otato !eetle"Coleotera, Chryso%elidae#& : Econ Ento%ol 8*6 );8-?2/&



Ar$entine :A, :M Clark and D+ =erro& (;8;!& 1elative fitness of insecticide-resistant Colorado otato !eetle strains "Coleotera6 Chryso%elidae#& EnvironEnto%ol (86?2/-?(2&

Ar$entine :A, 3 hu, S. >ee and :M Clark& (;;9& Bioche%ical-%echanis%s ofazinhos%ethyl resistance in iso$enic strains of Colorado otato !eetle& esticBioche% hysiol 986)-?8&

Ar$entine :A, S. >ee, MA Sos, S1 Barry and :M Clark& (;;/& er%ethrinresistance in a near iso$enic strain of Colorado otato !eetle& estic Bioche%hysiol /6;?-((/&

Baker MB and A. orter& *228& 7se of ser% recedence to infer theoverwinterin$ cost of insecticide resistance in the Colorado otato !eetles

"Coleotera6 Chryso%elidae#& A$ric =orest Ento%ol, in ress&

Baker MB, S1 Dastur, T <on$ and BD :affe& *228& Matin$ co%etition !etweenColorado otato !eetles "Coleotera6 Chryso%elidae# resistant or susceti!le toi%idaclorid does not show cost of resistance& Ann Ento%ol Soc A%, in ress&

Baker MB, D+ =erro and A. orter& *22(& Mana$e%ent of a well esta!lished cro est6 Colorado otato !eetle invasions on lar$e and s%all scales& Biol 'nvasions 6*;/-2)&

Baker MB, A Alyokhin, S1 Dastur, A. orter and D+ =erro& *22/& Ser% recedence in the overwintered Colorado otato !eetles "Coleotera6Chryso%elidae# and its i%lications for insecticide resistance %ana$e%ent& AnnEnto%ol Soc A% ;86;8;;;/&

Baker MB, A Alyokhin, A. orter, D+ =erro, S1 Dastur and + Galal& *22?&ersistence and inheritance of costs of resistance to i%idaclorid in Colorado

otato !eetle& : Econ Ento%ol (226(8?(-(8?;&

Benkovskaya G, MB 7dalov, AG +ikolenko and T> >eontieva& *22)& Te%oral

and toicolo$ical dyna%ics in the cover sot atterns of the Colorado otato !eetlein South 7ral& 1esist est Mana$e (/6(-(/&

Bethune C:S& (8?*& 1eort of the Ento%olo$ical Society of 5ntario for the year(8?(& .unter, 1oss, Toronto&

Biever 3D and 1> Chauvin& (;;2& rolon$ed dor%ancy in a acific +orthwest oulation of the Colorado otato !eetle, Leptinotarsa decemlineata "Say#"Coleotera6 Chryso%elidae#& Can Ento%ol (**6(?/-(??&

Bisho, BA and E: Grafius& (;;(& An on-far% insecticide resistance test kit forColorado otato !eetle "Coleotera6 Chryso%elidae#& A% otato : )86/-)9&



Bisho BA and E: Grafius& (;;)& 'nsecticide resistance in the Colorado otato !eetle& In6 :olivet and T. .siao& Chryso%elidae Biolo$y, olu%e (& SBAcade%ic u!lishin$, A%sterda%&

Blo% E, S =leischer and S%ilowitz& *22*& Satial and te%oral dyna%ics ofColorado otato !eetle "Coleotera6 Chryso%elidae# in fields with eri%eter andsatially tar$eted insecticides& Environ Ento%ol (6(9;-(/;&

Boiteau G& (;88a& Ser% utilization and ost-coulatory fe%ale-$uardin$ in theColorado otato !eetle, Leptinotarsa decemlineata. Ento%ol E Al 9?6(8-(8?&

Boiteau G& (;88!& Control of the Colorado otato !eetle, Leptinotarsadecemlineata "Say#6 learnin$ fro% the Soviet eerience& Bull Ento%ol Soc Can*26;-(9&

Boiteau G, 1. arry and C1 .arris& (;8?& 'nsecticide resistance in +ewBrunswick oulations of the Colorado otato !eetle "Coleotera6 Chryso%elidae#&Can Ento%ol ((;69/;-9)&

Boiteau G, elletier, GC Misener and G Bernard& (;;9& Develo%ent andevaluation of a lastic trench !arrier for rotection of otato fro% walkin$ adultColorado otato !eetles "Coleotera6 Chryso%elidae#& : Econ Ento%ol 8?6(*/-((&

Boiteau G, A Alyokhin and D+ =erro& *22& The Colorado otato !eetle in%ove%ent& Can Ento%ol (/6(-**&

Bour$uet D, M Des4uil!et and S >e%arie& *22/& 1e$ulatin$ insect resistance%ana$e%ent6 the case of non-Bt corn refu$es in the 7S& : Environ Mana$e ?)6*(2-**2&

Bour$uet D, A Genissel and M 1ay%ond& *222& 'nsecticide resistance anddo%inance levels& : Econ Ento%ol ;6(/88-(/;/&

Brown A<A& (;/(& Che%ical control of insects feedin$ on lants& In: 'nsectControl !y Che%icals& :ohn <iley, +ew ork, & /?9-))?&

Brust GE& (;;9& +atural ene%ies in straw-%ulch reduce Colorado otato !eetle oulations and da%a$e in otato& Biol Control 96()-();&

Bul%er MG and :: Bull& (;8*& Models of oly$enic se deter%ination and se ratioevolution& Evolution )6(-*)&

Cario MA& (;;8& Evaluatin$ resistance %ana$e%ent strate$ies for %ultile toins

in the resence of eternal refu$es& : Econ Ento%ol ;(6(2*(-(2(&



Cario M and E Grafius& (;;2& Effects of li$ht, te%erature and feedin$ status onfli$ht initiation in ostdiaause Colorado otato !eetle&Environ Ento%ol(;6*8(-*8/&

CarriVre and BE Ta!ashnik& *22(& 1eversin$ insect adatation to trans$enicinsecticidal lants& roc 1 Soc >ond B *)86(9?/-(982&

Carriere , C Ellers-3irk, 1 Bi$$s, B De$ain, D .olley, C afuso, Evans, T:Dennehy and BE Ta!ashnik& *22/& Effects of cotton cultivar on fitness costsassociated with of ink !ollwor% ">eidotera 6 Gelechiidae# to !t cotton& : EconEnto%ol ;86;9?-;/9&

Casa$rande 1A& (;8?& The Colorado otato !eetle6 (*/ years of %is%ana$e%ent&Bull Ento%ol Soc A% 6(9*-(/2&

Clark :M (;;?& 'nsecticides as tools in ro!in$ vital recetors and enzy%es inecita!le %e%!ranes& estic Bioche% hysiol /?6*/-*/9&

Clark :M, S. >ee, .: 3i%, 3S oon and AG han$& *22(& D+A-!ased$enotyin$ techni4ues for the detection of oint %utations associated withinsecticide resistance in Colorado otato !eetle Leptinotarsa decemlineata& estMana$e Sci /?6;)8-;?9&

Crow :=& (;/?& Genetics of insect resistance& Annu 1ev Ento%ol *6**?-*9)&

De 3ort CAD& (;;2& Thirty-five years of diaause research with the Colorado otato !eetle& Ento%ol E Al /)6(-(&

De <ilde :& (;98& Develoe%ent e%!ryonnaire et oste%!ryonnaire dydoryhore " Leptinotarsa decemlineata Say# en function de la te%erature& In6roceedin$s 8th 'nternational Con$ress of Ento%olo$y, Stockhol%, Sweden, &(2-*(&

De <ilde :& (;)*& The relation !etween diaause research and control of the

Colorado otato !eetle Leptinotarsa decemlineata Say& Ann Al Biol /26)2/-)28&

Denhol% ' and M< 1owland& (;;*& Tactics for %ana$in$ esticide resistance inarthroods6 theory and ractice& Annu 1ev Ento%ol ?6;(-((*&

Di=onzo CD, D< 1a$sdale, EB 1adcliffe, +C Gun%estad and GA Secor& (;;)&Cro !orders reduce otato virus incidence in seed otato& Ann Al Biol(*;6*8;-2*&

Din$le .& (;8/& Mi$ration& In: GA 3erkut and >' Gil!ert "eds&#, 'nsect hysiolo$y,

!ioche%istry, and har%acolo$y, vol& ;& er$a%on ress, 5ford, En$land, &?/-9(/&



Dively G, A =ollett, :: >induska and G3 1oderick& (;;8& 7se of i%idaclorid-treated row %itures for Colorado otato !eetle "Coleotera6 Chryso%elidae#%ana$e%ent& : Econ Ento%ol ;(6?)-8?&

=erro D+& (;;& otential for resistance to Bacillus thuringiensis6 Colorado otato !eetle "Coleotera6 Chryso%elidae# a %odel syste%& A% Ento%ol ;68-99&

=erro D+& (;;9& Biolo$ical control of the Colorado otato !eetle& In: G<ehnder, 13 :ansson, M> owelson, and 3 1a%an "eds#, Advances in otatoest Biolo$y and Mana$e%ent& AS ress, St& aul, & /?-?/&

=erro D+, :A >o$an, 1. oss and :S Elkinton& (;8/& Colorado otato !eetle"Coleotera6 Chryso%elidae# te%erature-deendent $rowth and feedin$ rates&Environ Ento%ol (969-98&

=erro D+, A= Tuttle and DC <e!er& (;;(& 5viositional and fli$ht !ehavior ofoverwintered Colorado otato !eetle "Coleotera6 Chryso%elidae#& EnvironEnto%ol *26(2;-((9&

=erro D+, A Alyokhin and DB To!in& (;;;& 1eroductive status and fli$htactivity of the overwintered Colorado otato !eetle&Ento%ol E Al ;(699-998&

=eyereisen 1& *22/& 'nsect Cytochro%e 9/2& In: > Gil!ert, 3 >atrou, and S Gill"eds#& Co%rehensive Molecular 'nsect Science& Elsevier, A%sterda%, Boston,

*-??&

=ollett A, GG 3ennedy and = Gould& (;;& A si%ulation %odel that eloresColorado otato !eetle "Coleotera6 Chryso%elidae# adatation to insecticides&Environ Ento%ol **6 *8-*;)&

=ollett A, = Gould and GG 3ennedy& (;;/& .i$h-realis% %odel of Colorado otato !eetle "Coleotera6 Chryso%elidae# adatation to er%ethrin& EnvironEnto%ol *96()?-(?8&

=or$ash A:& (;8/& 'nsecticide resistance in the Colorado otato !eetle& In: D+=erro and 1. oss "eds#, roceedin$s of the Sy%osiu% on the Colorado otatoBeetle, (?th 'nternational Con$ress of Ento%olo$y& Massachusetts Eeri%entStation, 7niversity of Massachusetts, A%herst, MA, & -/&

=rench +M ''', =ollett, BA +ault and GG 3ennedy& (;;& Colonization of otatofields in eastern +orth Carolina !y Colorado otato !eetle& Ento%ol E Al)86*9?-*/)&

Gauthier +>, 1+ .of%aster and M Se%el& (;8(& .istory of Colorado otato !eetle

control& In: :. >asho%! and 1 Casa$rande "eds#& Advances in otato estMana$e%ent& .utchinson 1oss u!lishin$ Co&, Strouds!ur$, A, & (-&



Goua%ene->a%ine, C+, 3S oon and :M Clark& *22& Differential susceti!ilityto a!a%ectin and two !ioactive aver%ectin analo$s in a!a%ectin-resistant and-susceti!le strains of Colorado otato !eetle, Leptinotarsa decemlineata "Say#"Coleotera 6 Chryso%elidae#& estic Bioche% hysiol ?)6(/-*&

Grafius E& (;;/& 's local selection followed !y disersal a %echanis% for raiddevelo%ent of %ultile insecticide resistance in the Colorado otato !eetleZ A%Ento%ol 9(6(29-(2;&

Grafius E& (;;?& Econo%ic i%act of insecticide resistance in the Colorado otato !eetle "Coleotera6 Chryso%elidae# on the Michi$an otato industry& : EconEnto%ol ;26((99-((/(&

Grafius E: and DS Douches& *228& The resent and future role of insect-resistant

$enetically %odified otato cultivars in otato 'M& In: : 1o%eis, AM Shelton,and GG 3ennedy "eds&#& 'nte$ration of 'nsect-1esistant GM cros within 'Mro$ra%s& Srin$er, +ew ork "in ress#&

.arcourt DG& (;?(& oulation dyna%ics of Leptinotarsa decemlineata "Say# ineastern 5ntario& '''& Ma0or oulation rocesses& Can Ento%ol (26(29;-(2)(&

.arris C1 and .: Svec& (;8(& Colorado otato !eetle resistance to car!ofuran andseveral other insecticides in Hue!ec Leptinotarsa decemlineata& : Econ Ento%ol?969*(-9*9&

.arris C1 and SA Turn!ull& (;8)& Contact toicity of so%e yrethroidsinsecticides, alone and in co%!ination with ieronyl !utoide, to insecticide-susceti!le and yrethroid-resistant strains of the Colorado otato !eetle"Coleotera6 Chryso%elidae# Can Ento%ol ((86((?-((?)&

.awthorne D:& *22(& A=>-!ased $enetic linka$e %a of the Colorado otato !eetle Leptinotarsa decemlineata6 Se chro%oso%es and a yrethroid-resistancecandidate $ene& Genetics(/86);/-?22&

.awthorne D:& *22& Huantitative trait locus %ain$ of yrethroid resistance inColorado otato !eetle, Leptinotarsa decemlineata "say# "Coleotera6Chryso%elidae#& : Econ Ento%ol ;)6(2*(-(22&

.ei% DC, GG 3ennedy and :< an Duyn& (;;2& Survey of insecticide resistancea%on$ +orth Carolina Colorado otato !eetle "Coleotera6 Chryso%elidae#

oulations& : Econ Ento%ol 86(**;-(*/&

.ei% DC, GG 3ennedy, => Gould and :< an Duyn& (;;*& 'nheritance offenvalerate and car!ofuran resistance in Colorado !eetles Leptinotarsa

decemlineata "Say# fro% +orth Carolina& estic Sci 962-((&



.itchner >S& (;/*& The 'nsecticide 'ndustry& In6 'nsects, the ear!ook ofA$riculture (;/*& .ouse Doc& 9(, <ashin$ton, DC, 9/2-9/?&

.of%aster 1+, 1> <aterfield and :C Boyd& (;)?& 'nsecticides alied to the soilfor control of ei$ht secies of insects on 'rish otatos in ir$inia& : Econ Ento%ol)26(((-((8&

.ou$h-Goldstein :A and :M <halen& (;;)& 1elationshi !etween cro rotationdistance fro% revious otatoes and colonization and oulation density ofColorado otato !eetle& : A$ric Ento%ol (6*;-22&

.ou$h-Goldstein :A, GE .ei%el, .E Bech%ann and CE Mason& (;;& Arthroodnatural ene%ies of the Colorado otato !eetle& Cro rotection (*6*9-9&

.oy C< and G .ead& (;;/& Correlation !etween !ehavioral and hysiolo$icalresonses to trans$enic otatoes containin$ Bacillus thuringiensis delta-endotoinin Leptinotarsa decemlineata "Coleotera6 Chryso%elidae#& : Econ Ento%ol886982-98)&

.oy C<, :A <y%an, TT au$hn, DA East and 3auf%an& (;;)& =ood, $roundcover, and Colorado otato !eetle "Coleotera6 Chryso%elidae# disersal in latesu%%er& : Econ Ento%ol 8;6;)-;);&

.ueth D and 7 1e$ev& (;?9& 5ti%al a$ricultural est %ana$e%ent with

increasin$ est resistance& A% : A$ric Econ /)6/9-//&

'nsecticide 1esistance Action Co%%ittee "'1AC#& *228& '1AC %ode of actionclassification, version /&(& htt6LLwww&irac-online&or$Ldocu%entsL'1AC*2MoA*2Classification*2v/[&df& >ast accessed (/Aril, *228&

'oannidis M, E Grafius and ME <halon& (;;(& atterns of insecticide resistanceto azinhos%ethyl, car!ofuran, and er%ethrin in the Colorado otato !eetle"Coleotera6 Chryso%elidae#& : Econ Ento%ol 896(9(?-(9*&

'oannidis, M, E: Grafius, :M <ieren$a, ME <halon and 1M .ollin$worth& (;;*&Selection, inheritance and characterization of car!ofuran resistance in the Colorado

otato !eetle "Coleotera, Chryso%elidae#& estic Sci /6*(/-***&

'sely D& (;/& ariations in the seasonal history of the Colorado otato !eetle& :3ansas Ento%ol Soc 86(9*-(9/&

:ac4ues 1>& (;88& The otato Beetles& E& :& Brill, >eiden&

:er%y T and G Sarin$er& (;//& A !ur$onya!o$ar " Leptinotarsa decemlineata Say#&

Mez\$azd 3iad], Budaest&



:ohnson CG& (;);& Mi$ration and Disersal of 'nsects !y =li$ht& Methuen and Co,>ondon&

:olivet & (;;(& The Colorado !eetle %enaces Asia " Leptinotarsa decemlineata Say(8*9#"Col& Chryso%elidae#& >JEnto%olo$iste 9?6 *;-98&3earsey M: and .S ooni& (;;)& The Genetical Analysis of Huantitative Traits&Cha%an and .all6 >ondon&

3i% .: and :M Clark& *22*& Evaluation of resistant oint %utations inreco%!inant acetylcholinesterase of Colorado otato !eetle& A!str aers A%Che% Soc **967(2-7(2&

3i% .:, D: .awthorne, T eters, G Dively and :M Clark& *22/& Alication ofD+A-!ased $enotyin$ techni4ues for the detection of kdr-like yrethroid

resistance in field oulations of Colorado !eetle& estic Bioche% hysiol 8(68/-;)&

3i% .:, :B Dunn, 3S oon and :M Clark& *22)& Tar$et site insensitivity and%utational analysis of acetylcholinesterase fro% a car!ofuran-resistant oulationof Colorado otato !eetle, Leptinotarsa decemlineata "Say#& estic Bioche%hysiol 896()/-(?;&

3i% .:, 3S oon and :M Clark& *22?& =unctional analysis of %utations ineressed acetylcholinesterase that result in azinhos%ethyl and car!ofuran

resistance in Colorado otato !eetle& estic Bioche% hysiol 886(8(-(;2&

3rishnan +, D 3odrik, = Turanli and = Sehnal& *22?& Sta$e-secific distri!ution ofoidative radicals and antioidant enzy%es in the %id$ut of Leptinotarsa

decemlineata& : 'nsect hysiol /6)?-?9&

>actin D: and .olliday +:& (;;9& Behavioral resonses of Colorado otato !eetlelarvae to co%!inations of te%erature and insolation, under field conditions&Ento%ol E Al ?*6*//-*)&

>asho%! :. and -S +$& (;89& Colonization !y the Colorado otato !eetle, Leptinotarsa decemlineata"Coleotera6 Cera%!ycidae# in rotated and non-rotated otato fields& Environ Ento%ol (6(/*-(/)&

>ee S and :M Clark& (;;)& Tissue distri!ution and !ioche%ical characterization ofcar!oylesterases associated with er%ethrin resistance in a near iso$enic strain ofColorado otato !eetle& estic Bioche% hysiol /)6*28-*(;&

>ee S. and :M Clark& (;;8& urification and characterization of %ultile-char$edfor%s of er%ethrin car!oylesterase"s# fro% the he%oly%h of resistant Colorado

otato !eetle& estic Bioche% hysiol )26(-9?&



>ee S., :B Dunn, :M Clark and DM Soderlund& (;;;& Molecular analysis of kdr-like resistance in a er%ethrin-resistant strain of Colorado otato !eetle& esticBioche% hysiol )6)-?/&

>evine E, . 5lou%i-Sade$hi and :1 =isher& (;;*& Discovery of %ultiyeardiaause in 'llinois and South Dakota +orthern corn rootwor% "Coleotera6Cera%!ycidae# e$$s and incidence of the rolon$ed diaause trait in 'llinois& :Econ Ento%ol 8/6*)*-*)?&

>iu B, BE Ta!ashnik, T: Dennehy, A> atin and AC Bartlett& (;;;& Develo%entti%e and resistance to Bt cros& +ature 9226/(;&

>iu <, MS <illia%son, S: >ansdell, : .an, ' Denhol% and +S Millar& *22)& Anicotinic acetylcholine recetor %utation "(/(S# causes reduced a$onist otency

to a ran$e of neonicotinoid insecticides& : +euroche% ;;6(*?-(*8(&

>o$an A, 1A Casa$rande, .. =au!ert and =A Dru%%ond& (;8/& Te%erature-deendent develo%ent and feedin$ of i%%ature Colorado otato

!eetles, Leptinotarsa decemlineata Say "Coleotera6 Chryso%elidae#& EnvironEnto%ol (96*?/-*8&

MacHuarrie C:3 and G Boiteau& *22& Effect of diet and feedin$ history on fli$htof Colorado otato !eetle, Leptinotarsa decemlineata. Ento%ol E Al (2?6*2?-*(&

May M>& (;8(& 1ole of !ody te%erature and ther%ore$ulation in the !iolo$y ofthe Colorado otato !eetle& In: :. >asho%! and 1 Casa$rande "eds#& Advances inotato est Mana$e%ent& .utchinson 1oss u!lishin$ Co&, Strouds!ur$, A, 8)-(29&

McCauley DE and >M 1eilly& (;89& Ser% stora$e and ser% recedence in the%ilkweed !eetle, Tetraopes tetraophthalmus "=orster# "Coleotera6Cera%!ycidae#& Ann Ento%ol Soc A% ??6/*)-/2&

McGau$hey < and ME <halon& (;;*& Mana$in$ insect resistance to Bacillusthuringiensis toins& Science */86(9/(-(9//&

Mc3enzie :A& *222& The character or the variation6 The $enetic analysis of theinsecticide-resistance henotye& Bull Ento%ol 1es ;26-?&

Milner M, 3:S 3un$, :A <y%an, : =eld%an and E +ordhei%& (;;*& Enhancin$overwinterin$ %ortality of Colorado otato !eetle "Coleotera6 Chryso%elidae# !y%aniulatin$ the te%erature of its diaause ha!itat& : Econ Ento%ol 8/6(?2(-(?28&



Minder '= and D etrova& (;))& Ecolo$ical and hysiolo$ical characteristics ofthe su%%er rest of the Colorado !eetle& In: 3 Arnoldi "ed&#& Ecolo$y andhysiolo$y of Diaause in the Colorado Beetle& +auka, Moscow, & */?*?;&

Misener GC, G Boiteau and > McMillan& (;;& A lastic-linin$ trenchin$ devicefor the control of Colorado otato !eetle6 Beetle Ecluder& A% otato : ?26;2-;28&

Miyo T, CB5 3eil, :A .ou$h-Goldstein and 5$u%a& (;;;& 'nheritance ofresistance to esfenvalerate in Colorado otato !eetles "Coleotera 6Chryso%elidae#& : Econ Ento%ol ;*6(2(-(28&

Moha%%adi Sharif M, M: .e0azi, A Moha%%adi and M1 1ashidi& *22?&1esistance status of the Colorado otato !eetle, Leptinotarsa decemlineata, to

endosulfan in East Azar!ai0an and Arda!il rovinces of 'ran& ?& : 'nsect Sci ?6(,availa!le online6 insectscience&or$L?&(&

Mota-Sanchez D *22& 1esistance and %eta!olis% of i%idaclorid in Coloradootato Beetle, Leptinotarsa decemlineta Say "Coleotera6 Chryso%elidae#, &(**,Ento%ol& Michi$an State 7niversity, East >ansin$&

Mota-Sanchez D, 1M .ollin$worth, E: Grafius and DD Moyer& *22)& 1esistanceand cross-resistance to neonicotinoid insecticides and sinosad in the Colorado

otato !eetle, Leptinotarsa decemlineata "Say# "Coleotera 6 Chryso%elidae#& est

Mana$e Sci )*62-?&

Mowry TM and >E Sandvol& (;;/& Survey of Colorado otato !eetle insecticideresistance in 'daho& A% otato : ?*6//(-//8&

+ational otato Council& *228& +eonicotinoid insecticides6 A $rower aroach toresistance %ana$e%ent of Colorado otato !eetle and $reen each ahid in otato&htt6LLwww&nationalotatocouncil&or$L+CLressroo%[newsflashes&cf%& >astaccessed ? Aril *228#&

+auen 1 and ' Denhol%& *22/& 1esistance of insect ests to neonicotinoidinsecticides6 Current status and future rosects& Arch 'nsect Bioche% hysiol/86*22-*(/&

+$ -S and :. >asho%!& (;8& 5rientation !y the Colorado otato !eetle" Leptinotarsa decemlineataSay#& Ani% Behav (6)(?-)(8&

+oronha C, GM Duke, :M Chinn and MS Goettel& *22(& Differential susceti!ilityto insecticides !y Leptinotarsa decemlineata "Coleotera6 Chryso%elidae#

oulations fro% western Canada& hytorotection 8*6((-(*(&



5lson E1, G Dively and :5 +elson& *222& Baseline susceti!ility toi%idaclorid and cross resistance atterns in Colorado otato !eetle "Coleotera6Chryso%elidae# oulations& : Econ Ento%ol ;6 99?-9/8&

our%irza AA& *22/& >ocal variation in susceti!ility of Colorado otato !eetle"Coleotera6 Chryso%elidae# to insecticide& : Econ Ento%ol ;86*(?)-*(82&Huinton 1:& (;//& DDT-resistant Colorado otato !eetlesZ roc +orth CentrEnto%ol Soc A% ;6;9-;/&

1ahard0a 7 and M E <halon& (;;/& 'nheritance of resistance to Bacillus

thuringiensis subsp. tenebrionisCry'''A delta-endotoin in Colorado otato !eetle"Coleotera6 Chryso%elidae#& : Econ Ento%ol 886*(-*)&

1ankin ME, M> McAnnely and :E Bodenha%er& (;8)& The oo$enesis-fli$ht

syndro%e revisited& In: < Danthanarayana "ed#, 'nsect fli$ht, disersal, and%i$ration& Srin$er-erla$, +ew ork, & *?-98&

1oderick G3, >G De Mendoza, G Dively and A =ollett& *22& Ser% recedence in Colorado otato !eetle, Leptinotarsa decemlineata "Coleotera6Chryso%elidae#6 Te%oral variation assessed !y neutral %arkers& Ann Ento%olSoc A% ;)6)(-))&

1ose 1> and <A Brindley& (;8/& An evaluation of the role of oidative enzy%es inColorado otato !eetle resistance to car!a%ate insecticides& estic Bioche% hysiol

*6?9-89&

Silco CA, GM Ghidiu and A&:& =or$ash& (;8/& >a!oratory and field evaluation of ieronyl !utoide as a yrethroid syner$ist a$ainst the Colorado otato !eetle"Coleotera6 Chryso%elidae#& : Econ Ento%ol ?86(;;-(92/&

Soderlund DM, C< .essney and MG :ian$& (;8& Meta!olis% of fenvalerate !yresistant Colorado otato !eetles adults& A!str aers A% Che% Soc (8)6*8-EST&

Sol!reck C& (;?8& Mi$ration, diaause, and direct develo%ent as alternative life

histories in a seed !u$, Neacoryphus bicruci& In: . Din$le "ed#, Evolution of 'nsectMi$ration and Diaause& Srin$er, +ew ork, &(;/-*(?&

Stankovic S, A a!el, M 3ostic, B Mano0lovic and S 1a0kovic& *229& Colorado otato !eetle R Leptinotarsa decemlineata "Say# resistance to or$anohoshates andcar!a%ates in Ser!ia& : est Sci ??6((-(/&

Ste$wee D, EC 3i%%el, :A de Boer and S .enstra& (;)& .or%onal control ofreversi!le de$eneration of fli$ht %uscle in the Colorado otato !eetle, Leptinotarsa

decemlineata Say "Coleotera#& : Cell Biol (;6/(;-/*?&



Stone B=& (;)8& A for%ula for deter%inin$ de$ree of do%inance in cases of%onofactorial inheritance of resistance to che%icals& Bull <.5 86*/-*)&

Stoner 3A& (;;& Effects of straw and leaf %ulches and srinkle irri$ation on thea!undance of Colorado otato !eetle "Coleotera6 Chryso%elidae# on otato inConnecticut& : Ento%ol Sci *86;-92&

Stewart :G, GG 3ennedy and A Sturz& (;;?& 'ncidence of insecticide resistance in oulations of Colorado otato !eetle, Leptinotarsa decemlineata "Say#"Coleotera6 Chryso%elidae#, on rince Edward 'sland& Can Ento%ol (*;6*(- *)&

Szentesi A& (;8/& Behavioral asects of fe%ale $uardin$ and inter-%ale conflict inthe Colorado otato !eetle& In: D+ =erro and 1. oss "eds#, roceedin$s of theSy%osiu% on the Colorado otato Beetle, (?th 'nternational Con$ress of

Ento%olo$y& Massachusetts Eeri%ent Station, 7niversity of Massachusetts,A%herst, MA, & (*?-(?&

Ta!ashnik BE& (;;9& Evolution of resistance to Bacillus thuringiensis& Annu 1evEnto%ol ;69?-?;&

Tan :G, D Mota-Sanchez, > Sal$ado and 1M .ollin$worth& *22/& Decreasednicotinic sensitivity to i%idaclorid as a resistance %echanis% in the Colorado

otato !eetle, Leptinotarsa decemlineata "SA#& A!str aers A% Che% Soc**;67)8-7)8&

Tan :G, Sal$ado and 1M .ollin$worth& *228& +eural actions of i%idaclorid andtheir involve%ent in resistance in the Colorado otato !eetle, Leptinotarsadecemlineata "Say#& est Mana$e Sci )96?-9?&

Tau!er M: and CA Tau!er& *22*& rolon$ed dor%ancy in Leptinotarsadecemlineata "Coleotera6 Chryso%elidae#6 a ten-year field study with i%licationsfor cro rotation& Environ Ento%ol (69;;-/29&

Trisyono A and ME <halon& (;;?& =itness costs of resistance to Bacillus

thuringiensis in Colorado otato !eetle "Coleotera6 Chryso%elidae#& : EconEnto%ol ;26*)?-*?(&

Trouvelot B& (;)& 1e%ar4ues sur lJecolo$ie du doryhore en (;/ dans le %assifcentral et le centre de la =rance& 1ev ool A$r Al */6 -?&

7shatinskaya 1S& (;)*& Colorado otato !eetle diaause and develo%ent of its%ulti-year infestations& ashchita 1astenii )6/-/9&

7shatinskaya 1S& (;))& rolon$ed diaause in the Colorado !eetle and conditions

of its develo%ent& In:3 Arnoldi "ed&#& Ecolo$y and hysiolo$y of Diaause inthe Colorado Beetle& +auka, Moscow, (*2(9&



lasova A& (;?8& A rediction of the distri!ution of Colorado !eetle in the Asiaticterritory of the 7SS1& ashchita 1astenii )699-9/&

oss 1. and D+ =erro& (;;2& henolo$y of fli$ht and walkin$ !y Colorado otato !eetle "Coleotera6 Chryso%elidae# adults in western Massachusetts& EnvironEnto%ol (;6((?-(**&

<al$en!ach := and :A <y%an& (;89& Colorado otato !eetle "Coleotera6Chryso%elidae# develo%ent in relation to te%erature in <isconsin& AnnEnto%ol Soc A% ??6)29-)2;&

<e!er DC and D+ =erro& (;;& Distri!ution of overwinterin$ Colorado otato !eetle in and near Massachusetts otato fields& Ento%ol E Al ))6(;(-(;)&

<e!er DC and D+ =erro& (;;9& Colorado otato !eetle6 diverse life history oseschallen$e to %ana$e%ent& In: G< ehnder, 13 :ansson, M> owelson, and 31a%an "eds#, Advances in otato est Biolo$y and Mana$e%ent& AS ress, St&aul, /9-?2&

<e!er DC and D+ =erro& (;;)& =li$ht and fecundity of Colorado otato !eetlesfed on different diets& Ann Ento%ol Soc A% 8;6*;?-2)&

<e!er D& *22& Colorado !eetle6 est on the %ove& estic 5utlook (96*/)-*/;&

<e$orek <& (;/?a& Badania nad !iolo$ia i ekolo$ia stonki zie%niaczane0" Leptinotarsa decemlineata Say#& 1oczn +auk 1oln ?9A*6 (/-(8/&

<e$orek <& (;/?!& Badania nad zi%ovanie% stonki zie%niaczane0 " Leptinotarsadecemlineata Say#& 1oczn +auk 1oln ?9A*6 ()-8&

<eisz 1, S%ilowitz and B Christ& (;;9& Distance, rotation, and !order crosaffect Colorado otato !eetle "Coleotera6 Chryso%elidae# colonization and

oulation density and early !li$ht " lternaria solani# severity in rotated otatofields& : Econ Ento%ol 8?6?*-?*;&

<eisz 1, S%ilowitz and S =leischer& (;;)& Evaluatin$ risk of Colorado otato !eetle "Coleotera6 Chryso%elidae# infestation as a function of %i$ratory distance&: Econ Ento%ol 8;69/-99(&

<halon ME and D+ =erro& (;;8& Bt-otato resistance %ana$e%ent& In: M Mellonand : 1issler "eds#, +ow or never6 serious new lans to save a natural est control&7CS, Ca%!rid$e, MA, & (2?-()&

<halon ME, D> Miller, 1M .ollin$sworth, E: Grafius and :1 Miller& (;;&

Selection of a Colorado otato !eetle "Coleotera6 Chryso%elidae# strain resistantto Bacillus thuringiensis. : Econ Ento%ol 8)6**)-*&



<halon ME, D Mota-Sanchez and 1M .ollin$worth& *228& The MS7 Arthrood esticide resistance data!ase& Availa!le online6 htt6LLwww&esticideresistance&or$&>ast accessed ? Aril, *228&

<ieren$a :M and 1M .ollin$worth& (;;*& 'nhi!ition of insect acetylcholinesterase !y the otato $lycoalkaloid -chaconine& +atur To (6;)-;;&

<ieren$a :M and 1M .ollin$worth& (;;& 'nhi!ition of alteredacetylcholinesterases fro% insecticide-resistant Colorado otato !eetles"Coleotera6 Chryso%elidae#& : Econ Ento%ol 8)6)?-)?;&

<ieren$a :M and 1M .ollin$worth& (;;9& The role of %eta!olic enzy%es ininsecticide-resistant Colorado otato !eetles& estic Sci 926*/;-*)9&

<ieren$a :M, D> +orris and ME <halon& (;;)& Sta$e-secific %ortality ofColorado otato !eetle "Coleotera6 Chryso%elidae# feedin$ on trans$enic otatoes& : Econ Ento%ol 8;6(29?-(2/*&

<iktelius S& (;8(& <ind disersal of insects& Grana *26*2/-*2?&

<orner S& (;88& Ecocli%actic assess%ent of otential esta!lish%ent of eotic ests& : Econ Ento%ol 8(6;?-;8&

<ri$ht 1:& (;89& Evaluation of cro rotation for control of Colorado otato !eetle

"Coleotera6 Chryso%elidae# in co%%ercial otato fields on >on$ 'sland& : EconEnto%ol ??6(*/9-(*/;&

an$ B& (;;9& Muscle develo%ent, ener$y source utilization, and %eta!olis%hor%one activity in Colorado otato !eetle, Leptinotarsa decemlineata "Say#fli$ht& M&S& Thesis, 7niversity of Massachusetts&

oon 3S, :5 +elson and :M Clark& *22*& Selective induction of a!a%ectin%eta!olis% !y dea%ethasone, -%ethylcholanthrene, and heno!ar!ital inColorado otato !eetle, Leptinotarsa decemlineata "Say#& estic Bioche% hysiol

?6?9-8)&

ehnder G<& (;8)& Ti%in$ of insecticides for control of Colorado otato !eetle"Coleotera6 Chryso%elidae# in eastern ir$inia !ased on differential susceti!ilityof life sta$es& : Econ Ento%ol ?;68/(-8/)&

ehnder G< and <D Gelernter& (;8;& Activity of the M-5+E for%ulation of anew strain of Bacillus thuringiensis a$ainst the Colorado otato !eetle "Coleotera6Chryso%elidae#6 relationshi !etween susceti!ility and insect life sta$e& : EconEnto%ol 8*6?/)-)(&



ehnder G< and : .ou$h Goldstein& (;;2& Colorado otato !eetle "Coleotera6Chryso%elidae# oulation develo%ent and effects on yield of otatoes with andwithout straw %ulch& : Econ Ento%ol 86(;8*-(;8?&

hao :, BA Bisho and E: Grafius& *222& 'nheritance and syner$is% of resistanceto i%idaclorid in the otato !eetle "Coleotera 6 Chryso%elidae#& : Econ Ento%ol;6(/28-(/(9&

hu 3 and :M Clark& (;;/& Clonin$ and se4uencin$ of a cD+A encodin$acetylcholinesterase in Colorado otato !eetle, Leptinotarsa decemlineata "Say#&'nsect Bioche% Mol Biol */6((*;((8&

hu 3 and :M Clark& (;;?& alidation of a oint %utation of acetylcholinesterasein Colorado otato !eetle !y oly%erase chain reaction couled to enzy%e assay&

estic Bioche% hysiol /?6*8-/&

hu 3, S. >ee and :M Clark& (;;)& A oint %utation of acetylcholinesteraseassociated with azinhos%ethyl resistance and reduced fitness in Colorado otato

!eetle& estic Bioche% hysiol //6(22-(28&

Documents

Colorado Potato Beetle Resistance to Insecticides