First records of parasitoids attacking the Asian citrus psyllid in Ecuador

RevistaBrasileiradeEntomologia61(2017)107–110

REVISTA

BRASILEIRA

DE

Entomologia

w w w . r b e n t o m o l o g i a . c o m

Short

Communication

First

records

of

parasitoids

attacking

the

Asian

citrus

psyllid

in

Ecuador

Diego

E.

Portalanza

_,

_Luis

_Sanchez

_,

_Marjorie

_Plúas

_,

_Imelda

_Felix

_,

_Valmir

_A.

_Costa

_,

Nivia

da

Silva

Dias-Pini

_,

_Sheryl

_{Ferreira-Stafanous}

_,

_Mariuxi

_L.

_{Gómez-Torres}

a_{AgenciaEcuatorianadeAseguramientodecalidaddelagro,Guayaquil,Ecuador} b_{InstitutoBiológico,Campinas,SP,Brazil}

c_{EmbrapaAgroindustriaTropical,Fortaleza,CE,Brazil}

d_{NewYorkCityDepartmentofEducation,NewYork,UnitedStates}

e_{MinisteriodeAgricultura,Ganaderia,AcuaculturayPesca–MAGAP,Quito,Ecuador}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received26May2016 Accepted19February2017 Availableonline6March2017

AssociateEditor:AdeneydeFreitasBueno Keywords: Diaphorencyrtusaligarhensis Diaphorinacitri Endoparasitoid Huanglongbing Tamarixiaradiata

a

b

s

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FirstrecordsofparasitoidsattackingtheAsiancitruspsyllidinEcuador.Theobjectiveofthecurrentstudy wastoinvestigatethepresenceofnaturalenemiesofDiaphorinacitri(Hemiptera:Liviidae)(theAsian cit-ruspsyllid)inEcuador.IncidenceofparasitoidDiaphorencyrtusaligarhensis(Hymenoptera:Encyrtidae) wasassessedbetweenNovember2015andMarch2016,inLetamendi,Febres-CorderoandTarqui,urban districtsofGuayaquil.Highestincidenceofparasitismoccurredinthoseregionsandseasonsoftheyear withthehighesttemperaturescommensuratewithincreaseofcitrusplantshoots.Similartotheirhost, theseparasitoidsappeartohaveestablishedinEcuadorbyaccident,andwerenottheresultof purpose-fulintroduction.ThisfortuitousintroductionisapotentiallyhelpfultoolincontrollingtheAsiancitrus psyllid,andpotentiallyHuanglongbing.

©2017SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Diaphorina citri Kuwayama (Hemiptera: Liviidae) is dis-tributedthroughoutSoutheastAsia,India,SaudiArabia,Mauritius and Reunion islands, Brazil, Uruguay (EPPO, 2014), Colombia

(Moncayo-Donosoetal.,2014),Ecuador(CornejoandChica,2014),

U.S.(Sétamouetal.,2008), Argentina,Venezuela,Mexicoandin

somecountriesoftheCaribbeanandCentralAmerica(EPPO,2014;

SENASICA,2012).

AmongD.citricatalogedhoststhereare25generainthe fam-ily Rutaceae,primarily Citropsis,Citrus and Murraya(Ikeda and

Ashihara,2008).Duetotheirdistributionandbiological

charac-teristicsitisthemostimportantvectorofhuanglongbing(HLB)or greening,themaincitrusdiseaseworldwide(Bove,2006;Wang

andTrivedi,2013).

Transmissionofpathogensbyarthropodsisaseriousproblem foragriculture.Inordertoaddresstheseagriculturalproblemsand tomaintainthequalityofagro-ecosystems,biologicalcontrol tac-ticsarebeingusedtoreducethepest.Theidiobiontectoparasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) and the arrhenotokous endoparasitoid Diaphorencyrtus aligarhensis

∗ Correspondingauthor.

E-mails:[email protected],[email protected]

(M.L.Gómez-Torres).

(Shaffee,AlamandAgarwal)(Hymenoptera:Encyrtidae)havebeen usedinprogramsofclassicalbiologicalcontroltothepopulation ofD.citriindifferentregionsoftheworld(Gómez-Torresetal.,

2006;Parraetal.,2007).

TamarixiaradiataisthemainagentofbiologicalcontrolofD. citri.Thisparasitoidhashighefficiencyofparasitismandagreat capacityfordispersal,establishment,andfield adaptation.Thus, thesuccessofT.radiatareleasesforbiologicalcontrolofD.citri, andconsequentlytheHLB,wasreportedintheReunion,Mauritius andGuadeloupeislands(Étienneetal.,2001),Taiwan(Chienetal.,

1991)andinUSA(Halletal.,2008).

Diaphorencyrtus aligarhensis preferentially parasitizes second andthirdinstarD.citri(Suleetal.,2014).Inadditionto parasiti-zation,femalescankillD.citrinymphs viahostfeeding(Rohrig etal.,2011).D.aligarhensishasbeenusedagainstD.citriin vari-ouscitrus-growingregionsincludingTaiwan,ReunionIsland,Saudi Arabia,andFlorida(Rohrigetal.,2012).FloridapopulationsofD. ali-garhensis,sourcedfromTaiwanandChina,havefailedtoestablish, despiterepeatedreleaseefforts(Rohrigetal.,2012;Bistline-East

etal.,2015).

DespitethepresenceofD.citribeingreportedinEcuadorsince

2014(CornejoandChica,2014),sofarnoparasitoidpopulations

have been detectedwhich might help to keep balance of this pest. Within this context, theaim of this study was tosurvey

http://dx.doi.org/10.1016/j.rbe.2017.02.002

0085-5626/©2017SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

108 D.E.Portalanzaetal./RevistaBrasileiradeEntomologia61(2017)107–110

Fig.1. DiaphorinacitrisurveysbetweenApril2013and2016.PointsrepresentmonitoredareasinGuayasprovince,Ecuador.Thelowerboxrepresentswheretheprovince islocated.

thepopulationofD.citriinEcuadorianregionswhereithasbeen reported,anddeterminevariationsamongpestpopulationsin dif-ferentseasonsandconsequentlyidentifytheparasitoidsassociated withthispsyllid.

Diaphorina citripopulation’s assessment in urban and rural

areasofGuayasprovince:

ToidentifyD.citri’sassociatedparasitoids,samplesweretaken inurbandistrictsinthecityofGuayaquil:Ximena(2◦1335S–79◦ 5345W),Febres-Cordero(2◦1145S–79◦5454W),Urdaneta (2◦ 12 08S–79◦ 54 20W), Rocafuerte (2◦ 11 16S–79◦ 52 44W), Tarqui (2◦ 09 52S–79◦ 56 14W), Chongon (2◦ 16 56S–80◦1108W),Letamendi(2◦1215S–79◦5412W),and other cities of Guayas province: El Empalme (0◦ 56 32S–79◦ 37 49W), Balzar (1◦ 17 36S–79◦ 52 49W),Colimes(1◦ 32 22S–79◦ 58 25W), SantaLucía (1◦ 41 30S–79◦ 5914 W), PedroCarbo(1◦4858S–80◦1822W),Daule(1◦5126S–79◦ 5208W),AlfredoBaquerizoMoreno(1◦5524S–79◦3231W), Milagro(2◦0901S–79◦3548W),Naranjal(2◦4041S–79◦38 24W),Balao(2◦5338S–79◦4112W)betweenApril2013and April2016atevery15days(Fig.1).

Ineachcase,acollectionwastakenfromtenbrancheswithbuds fromthirtyplantsshowingnymphsofD.citri.Thecollectionwas madebyfollowingaprotocolpreviouslydefinedandwithreference establishedbyGómez-Torresetal.(2006),samplesweretakenvery carefullyusingsecateursbeingcarefulnottodisturbtheinsects presentineachstratumuntilpackagingfortransport.

Thecollectedtwigswereplacedinpaperbags(30cm×15cm), properlylabeled,andconditionedat22±3◦CinaWaeco®electric

CoolerboxmodelCarFridge(17.5cm×31cm×31cm)wherethey weretransportedtothelaboratoryandimmediatelytransferredto acryliccages(35cm_×45cm_×35cm).Then,theyweredeposited onproperlysterilizedplastic trayscontainingamoistenedfilter paper sheet.For properconservation of the collectedmaterial, thelaboratorywasmaintainedat25±1◦C, relativehumidityof 80±10%anda12hphotophase.

Every 24h, the acrylic cages containing the nymphs were observedfortheextractionof emergedparasitoids,whichwere driedinacriticalpointdryer(LeicaCPD030)anddouble-mounted onpoints.ParasitoididentificationwasdoneaccordingtoNoyes

(1980)andHayat(1981)forgenusandtoShafeeetal.(1975)for

species.Thepercentageofemergencewas78.05.Thespecimens weredepositedatColec¸ãodeInsetosEntomófagosOscarMonte (Insti-tutoBiológico, Campinas,SãoPaulo,Brazil).Parasitoidscollected emerged onnymphs of D. citri were identified asD. aligarhen-sis.Female and male specimens of Tamarixia radiata werealso recorded.

Imagesoftheidentifiedmaterialtakenunderthestereoscopic microscopeandscanningelectronmicroscope(SEM)were exam-inedbyDr.JohnS.Noyes(NaturalHistoryMuseum,London,UK), whoconfirmedtheidentification.

Withtheseinitialstudiesin Ecuador,thevarious collections demonstratedthenaturalpresenceofparasitoidsD. aligarhensis and T. radiata in Letamendi, Febres-Cordero and Tarqui, urban districtsofGuayaquil(Fig.2).Thus, populationvariationsofthe pestandtheparasitoidmayoccuratdifferenttimesoftheyear, dependingonthe regionand themanagement. The absenceof

D.E.Portalanzaetal./RevistaBrasileiradeEntomologia61(2017)107–110 109

Fig.2.Letamendi,FebresCorderoandTarqui(triangles),GuayaquilcityurbandistrictswhereDiaphorencyrtusaligarhensiswasdetected.Thelowerboxrepresentswhere thecityislocated.

naturalenemies,insomelocalities,couldbedirectlyrelatedtothe indiscriminateapplicationofchemicalsusedtocontrolinsectsand mites,aswellasD.citri.

Establishmentof this parasitoidin othercountries of South Americahasnotbeenreported.SimilartoD. citri,the endopar-asitoid D. aligarhensis appears to have established in Ecuador accidentally,andwerenottheresultofpurposefulintroduction. Itisnotunusualforthisparasitoidtobediscoveredinnon-release locationsinHawaii(Matsunaga,2014).

This workfits within the objectives of the national plan of wellliving ofEcuador(SumakKawsay)2012–2017Article7“To guaranteetherightsofnatureandtopromoteenvironmental sus-tainability”.With this record the possibility ofadopting a new tacticforsustainablemanagementofD.citriandthusmaintainan ecologicalbalancethat allowssustainableand economicallyfair agricultureopens.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

ToDr.JohnS.Noyes(NaturalHistoryMuseum,London,UK),for thehelpontheidentificationofDiaphorencyrtusaligarhensis.To the“InstitutoNacionaldeCiênciaeTecnologiadosHymenoptera ParasitoidesdaRegiãoSudesteBrasileira(INCT-HymparSudeste)”, forfinancialsupporttooneoftheauthors(VAC).ToEng.Javier Contreras(AGROCALIDAD)fortechnicalsupport.

WeexpressheartfeltthankstoJavierPonce,Ministrode Agricul-tura,Ganadería,AcuaculturayPescadelEcuadorfortheirsupportin creatingtheReddeExpertosenProtecciónVegetal(MAGAP-REPV).

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