RevistaBrasileiradeEntomologia60 (2016)101–104
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REVISTA
BRASILEIRA
DE
Entomologia
AJournalonInsectDiversityandEvolutionShort
Communication
Timeline
and
geographical
distribution
of
Helicoverpa
armigera
(Hübner)
(Lepidoptera,
Noctuidae:
Heliothinae)
in
Brazil
Daniel
R.
Sosa-Gómez
a,∗,
Alexandre
Specht
b,
Silvana
V.
Paula-Moraes
b,
Adilson
Lopes-Lima
c,
Silvia
A.C.
Yano
a,
Adriana
Micheli
a,
Elisangela
G.F.
Morais
d,
Paulo
Gallo
a,
Paulo
R.V.S.
Pereira
e,
José
R.
Salvadori
f,
Marcos
Botton
g,
Maurício
M.
Zenker
h,
Wilson
S.
Azevedo-Filho
iaEmbrapaSoja,Londrina,PR,Brazil bEmbrapaCerrados,Planaltina,DF,Brazil cEmbrapaAmapá,Macapá,AP,Brazil dEmbrapaRoraima,BoaVista,RR,Brazil eEmbrapaTrigo,PassoFundo,RS,Brazil
fFaculdadedeAgronomiaeMedicinaVeterinária,UniversidadedePassoFundo,PassoFundo,RS,Brazil gEmbrapaUvaeVinho,BentoGonc¸alves,RS,Brazil
hDepartamentodeZoologia,InstitutodeBiologia,UniversidadeEstadualdeCampinas,Campinas,SP,Brazil
iLaboratóriodeBiologia,CentrodeCiênciasExatas,daNaturezaedeTecnologia,UniversidadedeCaxiasdoSul,BentoGonc¸alves,RS,Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:Received3November2014 Accepted21September2015 Availableonline19December2015 AssociateEditor:AdeneyF.Bueno Keywords:
OldWorldbollworm Polyphagouscaterpillar Geographicaldistribution
a
b
s
t
r
a
c
t
ThisstudypresentsregistersofHelicoverpaarmigera(Hübner)occurrencetoassessitsspatialand tempo-raldistributioninBrazil.Weuseddatafromcollections,especiallyfromtheSouthernRegion,systematic collectionsinRioGrandedoSul,occasionalcollectionsofcaterpillarsandadultsindifferentregionsof Brazil,aswellasliteratureregisters.WeconcludethattheintroductionofH.armigerainBrazilprobably occurredbeforeOctober2008.WealsoregisterthatinAugust2012H.armigerawasalreadypresentfrom theextremesouthernpart(RioGrandedoSul)totheextremenorthernpart(Amapá)ofBrazil.
PublishedbyElsevierEditoraLtda.onbehalfofSociedadeBrasileiradeEntomologia.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
InMarch2013,theOldWorldbollworm,Helicoverpaarmigera (Hübner),wasreportedinBrazil(Embrapa,2013).Onthat occa-sion,specimenswerecollectedinthestatesofBahia,MatoGrosso, Paraná,andGoiás,andalsoinDistritoFederal,causingdamageon corn,soybean,andcotton(Czepaketal.,2013;Spechtetal.,2013b). Theidentificationwasbasedonmorphologicalcharactersofmale genitalia(Czepaketal.,2013;Spechtetal.,2013b)and molecu-laranalysis(Spechtetal.,2013b).Thisspeciesisgeneticallyand morphologicallycloselyrelatedtoHelicoverpazea(Boddie),andthe identificationbasedongenitaliacharactersistime-consumingand requiresawell-trainedtaxonomist.Thesetwospeciesarealmost indistinguishablewhencharacterizationisbasedonexternal mor-phologicalcharacters(Hardwick,1965;Pogue,2004;Spechtetal., 2013b).For thesereasons,surveyswereperformed indifferent partsofthecountrytoconfirmthegeographicaldistribution,using reliablediagnosticmethods(innermalegenitaliaand/ormolecular
∗ Correspondingauthor.
E-mail:daniel.sosa-gomez@embrapa.br(D.R.Sosa-Gómez).
tools),andestablishtheapproximatetimeofintroductionofthis pestinBrazil.
The geographical distribution wasobtainedafter identifying fieldcollectedlarvae,orrearingimmaturesuntiltheadultphase, orcollectingowletmothswithlighttraps.TheoccurrenceofH. armigerabefore2013inBrazilwasinvestigatedthroughanalysis ofsamplesdepositedinscientificcollectionsfromEmbrapa Cer-rados,EmbrapaSoybean,theMuseumofScienceandTechnology fromPontifíciaUniversidadeCatólicadoRioGrandedoSul(PUCRS), andthecollectionoftheUniversidadedeCaxiasdoSul, consider-ingmainlythesamplescollectedusinglighttrapsinRioGrande doSulsince1998(TestonandCorseuil,2004;Spechtetal.,2005, 2013a;Zenkeretal.,2010)andsystematizedmonthlycollections usinglighttraps,fromMay2011toApril2013,inPintoBandeira,RS. Themorphologicalandmolecularidentificationswereperformed asdescribedbyPogue(2004)andBehereetal.(2008).
The PCR-RFLP molecular analysis, was performed with the amplificationproductcorrespondingtopositions between2443 and 2953from the COI gene of Helicoverpa species (Accession numberGU188273fromH.armigeramitogenome)andrestriction
http://dx.doi.org/10.1016/j.rbe.2015.09.008
0085-5626/PublishedbyElsevier EditoraLtda. onbehalf ofSociedade Brasileirade Entomologia.This is anopenaccess articleunderthe CCBY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
102 D.R.Sosa-Gómezetal./RevistaBrasileiradeEntomologia60(2016)101–104
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30
Fig.1.PCR-RFLPagarosegel(1.5%)forCOIamplificationproducts(511b)usingBstZ17Iendonuclease.Lane1:100bpMW;lanes2and5:undigestedproductofHelicoverpa zea(Londrina,PR);lanes3and4:digestionproductofHelicoverpaarmigera(Londrina,PR);lane6:digestionproductofH.armigera;lanes7–10:undigestedproductofH.zea (Planaltina,DF);lanes11–15:digestionproductofH.armigera(LuizEduardoMagalhães,BA);lanes16–20:digestionproductofH.armigera(Carambeí,PR);lanes21and22: undigestedproductofH.zea(Arapoti,PR);lanes23and24:digestionproductofH.armigera(Sengés,PR);lanes25–28:digestionproductofH.armigera(Taquarituba,SP); lane29:undigestedproductofH.zea(Taquarituba,SP);lane30:100bpMW.
Table1
Helicoverpaspp.inBrazilcollections.
Brazilianmunicipalities/states Geographiccoordinates(UPS) Plantortrapcollect Species Samplingdate Identification BoaVista,Roraima 02◦5345N;60◦3942W Soybean H.armigera 05/08/2013 Morphological
Bonfim,Roraima 03◦1955N;59◦5044W Soybean H.armigera 05/08/2013 Morphological
Bonfim,Roraima 03◦1955N;59◦5044W Corn H.armigera,H.zea 05/08/2013 Morphological
Macapá,Amapá 00◦1448S;51◦1754W Soybean H.armigera 08/08/2012 Morphological
BaixadaGrandedoRibeiro,Piauí 07◦5101S;45◦1249W Cotton H.armigera 12/05/2013 Morphological
LuísEduardoMagalhães,Bahia 12◦0712S;45◦4841W Cotton, H.armigera,H.zea 06/2012 Molecular,morphological LuísEduardoMagalhães,Bahia 12◦0712S;45◦4841W Soybean H.armigera 06/2012 Molecular,morphological RodaVelha,Bahia 12◦429S;45◦4930W Cotton,Soybean H.armigera 21/02/2013 Morphological
Correntina,Bahia 13◦2733S;45◦4411W Cotton H.armigera,H.zea 23/12/2012 Morphological
Correntina,Bahia 13◦2733S;45◦4411W Soybean H.armigera 23/12/2012 Morphological
NovaMutum,MatoGrosso 13◦5359S;55◦4753W Soybean H.armigera 23/02/2013 Morphological
Diamantino,MatoGrosso 14◦2129S;56◦2312W Soybean H.armigera 21/01/2013 Morphological
TangarádaSerra,MatoGrosso 14◦3744S;57◦3432W Soybean H.armigera 06/03/2013 Morphological CampoVerde,MatoGrosso 15◦2819S;55◦0840W Soybean H.armigera 08/02/2013 Morphological Rondonópolis,MatoGrosso 16◦4243S;54◦3943W Cotton H.armigera 11/04/2013 Morphological
AltoTaquari,MatoGrosso 17◦5008S;53◦2746W Soybean H.armigera 14/01/2013 Morphological
PalmeiradeGoiás,Goiás 16◦3929S;49◦5613W Soybean H.armigera 23/02/2013 Morphological
Jataí,Goiás 17◦5625S;51◦4746W Soybean H.armigera 23/02/2013 Morphological
SantaJuliana,MinasGerais 19◦2129S;47◦2836W Cowpea H.armigera 23/02/2013 Morphological
AfonsoCláudio,EspirituSanto 20◦0255S;41◦0618W Tomato H.armigera 02/03/2014 Morphological Alegre,EspíritoSanto 20◦4545S41◦3228W Tomato H.armigera 02/03/2014 Morphological Planaltina,DistritoFederal 15◦3505S;47◦5314W Corn,soybean H.zea,H.armigera 03/10/2013 Molecular,morphological
Planaltina,DistritoFederal 15◦3505S;47◦5314W soybean H.armigera 03/10/2013 Molecular,morphological
Brasília,DistritoFederal 15◦4406S;47◦5314W Tomato H.armigera,H.zea 20/11/2013 Morphological
CostaRica,MatoGrossodoSul 18◦3449S;53◦0908W Soybean H.armigera 21/12/2013 Morphological
Londrina,Paraná 23◦1144S;51◦1034W Soybean,lighttrap H.armigera,H.zea 07/02/2013 Molecular,morphological Rolândia,Paraná 23◦1747.0S51◦2601.9W Soybean H.armigera 10/14/2008 Molecular
Taquarituba,SãoPaulo 23◦4249S;49◦1140W Soybean H.armigera 03/27/2013 Molecular
Sengés,Paraná 24◦0722S;49◦2854W Soybean H.armigera 03/27/2013 Molecular
Arapoti,Paraná 24◦1152S;49◦5512W Wheat H.zea 03/27/2013 Molecular
Carambei,Paraná 24◦5936S;50◦0827W Soybean H.armigera 03/27/2013 Molecular,morphological
PassoFundo,RioGrandedoSul 28◦2255S;52◦3896W Soybean H.armigera,H.zea 20/12/2012 Morphological
PintoBandeira,RioGrandedoSul 29◦0250S;51◦2812W Lighttrap H.armigera 04/05/2011 Morphological Espumoso,RioGrandedoSul 28◦4311S;52◦4716W Soybean H.armigera 21/12/2012 Morphological Carazinho,RioGrandedoSul 28◦2026S;52◦5257W Soybean H.armigera,H.gelotopoeon 20/12/2012 Morphological
fragmentlengthpolymorphism (RFLP)analysiswiththeBstZ17I endonuclease(Fig.1),aswellasthemorphologicalcharacters indi-catethatsofarH.armigeraoccursinthefollowingstatesofBrazil: Roraima,Amapá,Piauí,Bahia,MatoGrosso,MatoGrossodoSul, DistritoFederal,Goiás,EspíritoSanto,SãoPaulo,Paraná,andRio GrandedoSul(Table1andFig.1).
WeidentifiedoneH.armigeraspecimeninalarvalsample col-lectedinRolândia,Paraná,inOctober14,2008.Thiswasthefirst timethatthisspecieswasobservedinsamplesanalyzedforthe presentstudy.Afterthis,theexam ofadultsfromsystematized monthlycollectionsinPintoBandeira,RS(extremesouthernBrazil)
providedthedetectionofH.armigeraonMay4,2011.Inthesame year,H.armigeraspecimenswerecollectedinAugust(n=6)and September(n=1).In 2012,adultsof H.armigerawerefoundin February(n=1),August(n=4),September(n=3),October(n=1), andDecember(n=1).In2013,adultsofthisspecieswerecollected inFebruary(n=2),March(n=2),andApril(n=4).
TheexamofadultsobtainedfromimmaturesofH.armigera col-lectedinsoybeanfieldsintheextremenorthernBrazil(Amapá) confirmedtheoccurrenceofthisspeciessinceAugust8,2012.Most ofHeliothinaelarvaecollectedinsoybeanfieldswereH.armigera, averysmallproportionofspecimensbelongtoChlorideavirescens
D.R.Sosa-Gómezetal./RevistaBrasileiradeEntomologia60(2016)101–104 103
(0.2%).Evaluationsofcollectionsperformedfrom1998(Testonet al.,2006)until2008(Zenkeretal.,2010;Spechtetal.,2013a)in theSouthernRegionofBrazildidnotrevealtheoccurrenceofH. armigera.WedidnotfindH.zeaspecimensfromimmatureinsects collectedin soybean.However,this formerspeciesis asoybean pestinUnitedStateofAmerica(Swensonetal.,2013).Allthe Heli-coverpasamplescollectedfromcornwereobtainedfromcornear, revealinghostpreferenceofBrazilianpopulationsofH.zeaforthis hostplant.
Theanalysisofinsects previouslycollectedanddeposited in museumsbyseveralauthors(TestonandCorseuil,2004;Specht etal.,2005,2013a;Zenkeretal.,2010)suggestedthatatleastin RioGrandedoSultheintroductionofH.armigeraoccurredafter December2008andbeforeMay2011.TheearliestH.armigera sam-plesmentionedinthepublishedliteraturearefromMay22,2012 (Leiteetal.,2014)inthisstudywefoundonelarvaeofH.armigerain soybeanfieldsfromRolândia,ParanáinOctoberof2008.Basedon theevidenceprovidedbythesedataandconsideringascenarioof introductionofH.armigerainthecountrybefore2008,itis reason-abletoinferthatthispesthadenoughtimetobuilduppopulations detectedasoutbreaksinthe2012/2013growingseason(Embrapa, 2013).InAugust2011,sixspecimenswerecapturedinone samp-lingdate,indicatingthatpopulationsofthisinsectwerealready establishedinthisarea.Interestingly,intwoconsecutiveyearsof monthlysamplingaprogressiveincreaseofadultscapturedmainly attheendofthewinter(AugustandSeptember)andattheendof thesummer(April)wasobserved.
ThefactthatH.armigerawasdetectedfromnorthernto south-ernBrazil,atleastduringthe2012/2013growingseason,when substantialdamagewasreportedbyseveralresearchers(Czepak etal.,2013;Spechtetal.,2013b;Tayetal.,2013),revealsthatthe identificationofthisspeciesinthecountrywascarriedoutalong timeafteritsintroduction,constrainingmanagementcontrol deci-sionstominimizetheimpactofthispestinseveralcrops.Soonafter beingreportedinBrazil,H.armigerawasalsofoundinParaguay and Argentina (Senave, 2013; Murúa et al., 2004), Puerto Rico (NorthAmericanPlantProtectionOrganization,2014)andlaterin USA ( http://www.freshfromflorida.com/Divisions-Offices/Plant- Industry/Plant-Industry-Publications/Pest-Alerts/Pest-Alert-The-Old-World-Bollworm).
Thelatedetection ofH.armigeraafteritsintroductioncould beattributedtothehighsimilaritybetweenthis speciesandH. zea, as wellas to thescarce number of studies for the identi-ficationof pestspecies,suchasinsectidentificationguides and otherrelated publications (Hoffmann-Campoet al.,2012; Sosa-Gómezetal.,2014).Moreover,thespecificidentificationofinsect speciesiscarriedout,almostexclusively,basedonexternal mor-phologyoftheadultspecimens,whichrequiresrearingimmature individuals.Thistechniqueistime consumingand,manytimes, natural enemies kill the immature individuals. Therefore, only some studiesof theimmature stages of insects (Angulo et al., 2008)andspeciesidentificationusingmolecularmarkers( Gomez-Rolimetal.,2013),whichrequiresmoreinvestments,especially inequipmentandspecializedtechnicians,havebeenperformed. However,mostofthesestudiesfocusondeterminedtaxa,usually genera,andmostspecies continue nothavinga complete mor-phological or molecularcharacterization.These deficiencies are evidenced in many countries, especially in South America, due toabiological megadiversity andlackof taxonomists(Marques and Lamas, 2006). Furthermore, the morphological similarities between H. armigera and H. zea turn the situation even more critical.
In conclusion, the detection of H. armigeraas a devastating componentin high-valuecommercialcrops,suchascottonand soybean(Czepaketal.,2013;Spechtetal.,2013b),showsthe vul-nerabilityofBrazilandothercountriesinSouthAmericaregarding
quarantinepests.Additionally,effortstoelucidateinvasionpaths andoriginareessentialtodesignstrategiesforpreventingfuture pestintroductionandadoptingscience-basedpolicies(Estoupand Guillemaud,2010;Guillemaudetal.,2011).
Conflictsofinterest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgments
TheauthorsthankConselhoNacionaldeDesenvolvimento Cien-tíficoeTecnológico(CNPq)forthefinancialassistance(Processes 403376/2013-0, 476691/2013-3) and José Jairo da Silva for his assistancewithmoleculartechniques.
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