RevistaBrasileiradeEntomologia61(2017)290–293
REVISTA
BRASILEIRA
DE
Entomologia
AJournalonInsectDiversityandEvolutionw w w . r b e n t o m o l o g i a . c o m
Biology,
Ecology
and
Diversity
First
record
of
Heteropsylla
caldwelli
Burckhardt
(Hemiptera:
Psyllidae)
from
Brazil
and
its
population
dynamics
on
earpod
tree
in
Rio
Grande
do
Sul
Leonardo
Mortari
Machado
a,∗,
Daniel
Burckhardt
b,
Dalva
Luiz
de
Queiroz
c,
Ervandil
Corrêa
Costa
a,
Dayanna
do
Nascimento
Machado
a,
Leandra
Pedron
aaUniversidadeFederaldeSantaMaria,SantaMaria,RS,Brazil bNaturhistorischesMuseum,Basel,Switzerland
cEmbrapaFlorestas,Colombo,PR,Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:Received22May2017
Accepted13July2017 Availableonline27July2017 AssociateEditor:DouglasZeppelini Keywords: Distribution Fabaceae Hostplant Jumpingplant-lice Neotropical
a
b
s
t
r
a
c
t
HeteropsyllacaldwelliBurckhardt(Psyllidae,Ciriacreminae)isreportedforthefirsttimefromBrazil (StatesofMinasGerais,Paraná,RioGrandedoSul)fromEnterolobiumcontortisiliquum(Vell.)Morong. Theearpodtree,fromAlbiziaedwallii(Hoehne)BarnebyandJ.W.GrimesandSenegaliapolyphylla(DC.) Britton(Fabaceae,Mimosoideae),allpreviouslyunknownhosts.Thepopulationdynamicsofthepsyllid wereinvestigatedinaseven-year-oldplantationofE.contortisiliquuminanabandonedopen-pitcoalmine inCandiota,RioGrandedoSulduringtwoyears.Thepopulationshowedpeaksinspringandsummer, correlatingdirectlywiththemeanairtemperatureandthepopulationsizeofmicrohymenoptera.
©2017SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
ThegenusHeteropsyllacomprises40speciesofplant-sap suck-ing insects occurring from the southern United States in the northtoNorthern Argentina andChile in thesouth, which are monophagousoroligophagousonmimosoidFabaceae(Hodkinson
andMuddiman,1993;Muddimanetal.,1992).Species
identifica-tionisoftendifficultasmorphologicaldifferencesbetweensome speciesaresmall.
Somespecies, e.g.HeteropsyllacubanaCrawford,Heteropsylla huasachaeCaldwellandHeteropsyllamimosaeCrawford,have sig-nificantlyexpandedtheirnaturalgeographicalranges.Thespread ofH.cubana,associatedwithLeucaenaspp.,isparticularly spec-tacular.FromitsorigininMexico,CentralAmerica,theCaribbean andnorthernSouthAmerica,itspreadaroundtheworldwithin adecadeviaHawaii,SoutheastAsia,AustraliaandIndiato tropi-calAfrica(Alénéetal.,2012;Muddimanetal.,1992).Thespecies canbecomeaseverepestwhereLeucaenaisintentionallyplanted. InsomeareasLeucaenaleucocephala(Lam.) deWithasescaped cultivationandisconsideredaninvasiveweed.There,H.cubana
∗ Correspondingauthor.
E-mail:[email protected](L.M.Machado).
mayhelptocontrolitsspread(Walton,2003).Anotherspecies,the BrazilianHeteropsyllaspinulosaMuddiman,Hodkinsonand Hod-kinson,hasbeenintroducedintoQueenslandandWesternSamoa tocontrolMimosadiplotrichaC.WrightexSauvalle(Willsonand
Garcia,1992).
Speciesdiversity,distributionandhostassociationswithinthe genus Heteropsyllaare well documented for North and Central America but less for tropical South America (Muddiman et al., 1992).Inparticular,littleisknownfromBrazilfromwhereonly threespecieshavebeenreported:H.cubana,asintroductionon Leu-caenaspp.,H.spinulosafromM.diplotrichaandHeteropsyllatenuata Muddiman,HodkinsonandHodkinsonpossiblyfromEnterolobium contortisiliquum(Vell.)Morong(BurckhardtandQueiroz,2012).
FormostBrazilianpsyllidspecies,littleisknownabouttheir populationdynamics(BurckhardtandQueiroz,2012).Exceptions areintroducedinsectpestssuchastheeucalyptpsyllids(Santana etal.,2009).Someinformationisalsoavailableforgallinducing species (Carneiro et al., 2013).H.cubana and H. spinulosa,two fairlywell-studiedspecies,arepolyvoltineandoverwinterasegg, immatureoradultontheirhost(Hodkinson,2009).Polyvoltinism iscommonintropicalandSouthtemperatepsyllidspecieswith free-livingimmatures.
The earpod tree, E.contortisiliquum, ranges from Argentina, Uruguay,Paraguay,southern,centralandeasternBraziltoBolivia
http://dx.doi.org/10.1016/j.rbe.2017.07.003
0085-5626/©2017SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http://
L.M.Machadoetal./RevistaBrasileiradeEntomologia61(2017)290–293 291
Fig.1. Psyllidssamplingwithabeatingnetinthemiddleinaseven-year-old plantationofEnterolobiumcontortisiliquuminanabandonedopen-pitcoalminein Candiota,RS,betweenMay2014andApril2016.
andisutilisedforavarietyofpurposes.Itisplantedasshadetree instreetsandgardensaswellasinagroforestrysystems,e.g.,for cocoaandyerbamate.Itsrapidgrowthandnitrogen-fixingabilities makeitusefulforrevegetation,soilstabilisationandimprovement, aswellaslandreclamation.Itistolerantofcopper-contaminated soil.Thetreeisalsoharvestedforitstimberandmedicinaluses, andthefoliageiseatenbycattle(Praciaketal.,2013).
Recently,asecondHeteropsyllaspecieswasdiscoveredonE. con-tortisiliquuminBrazil,i.e.Heteropsyllacaldwelli,a specieswhich developsalsoonAlbiziaadinocephala(Donn.Sm.)BrittonandRose andEnterolobiumcyclocarpum(Jacq.)Griseb.OriginallyH.caldwelli wasdescribedfromArgentina andParaguay (Burckhardt,1987) andsubsequentlyreportedfromPanama(BrownandHodkinson, 1988),Colombia,CostaRica,Trinidad(Muddimanetal.,1992)and Nicaragua(Maesetal.,1993).HerewereportH.caldwelliforthefirst timefromBrazil(StatesofMinasGerais,Paraná,RioGrandedoSul), listnewhost-plantsanddiscussitspopulationdynamicsinrelation tosomeabiotic(meanairtemperatureandprecipitation)andbiotic (predatorandparasitoids)factorsbasedonatwo-yearstudyofthe speciesinaseven-year-oldplantationofE.contortisiliquuminan abandonedopen-pitcoalmineinRioGrandedoSul.
Materialandmethods
Material
In the context of a larger project on the psyllid fauna of Brazil,DB and DLQprospectedover 200localities in14 Brazil-ianstatesfrom2010to2017.Thespecimenswerecollectedinto 70%ethanolusingasweepnetandaspirator(Queirozetal.,2017). ThematerialisdepositedintheNaturhistorischesMuseumBasel, Switzerland(NHMB),theLaboratóriodeEntomologia,Embrapa Flo-restas,Colombo,PR,BrazilandtheMuseudeZoologia,Universidade de São Paulo, SP, Brazil. Specimens, including paratypes, of H. caldwellifromArgentina,Colombia, Panamaand Paraguaywere examinedfromthecollectionsoftheMuséumd’histoirenaturelle, Genève,Switzerland,andtheNHMB.
Thesamplesfor thestudyof thepopulationdynamicswere takenbyLMMfromMay2014toApril2016inmonthlyintervals withabeatingnetbearingafunnelattachedinthemiddle(Fig.1). Everymonth,20samplesweretakenbyinsertingthenetintothe foliagewhichwasthenshakententimes.Thepsyllidsretainedin thecollectingfunnelwerestoredinplasticbags,labelledandthen sortedandidentifiedintheLaboratoryofForestEntomologyofthe
FederalUniversityofSantaMaria,RS,Brazil.Theidentificationsof somepsyllidsampleswerecheckedbyDB(samplesdepositedin NHMB).
Populationdynamics
Thesite, where thepopulationdynamicsofH. caldwelliwas studied,islocatedinthemunicipalityofCandiota,S31◦33.3and W53◦42.9 at 270masl,StateofRio GrandedoSul,Brazil.The areaispartofthePampabiome,whichextendsfromthe south-ernhalfofRioGrandedoSulinBraziltotheProvinceofMisiones inArgentina.Theaverageannualrainfallis1414mm,with rain-fallpredominantlyinSeptemberandOctober,correspondingtoa Cfaclimatetype,i.e.,humidsubtropical,withhotsummer(Alvares etal.,2014).Themeantemperatureinthecoldestmonthisbelow 18◦C,thatofthehottestmonth22◦C(Moreno,1961).
Theearpodtreesthatwestudiedwereseven-years-oldwhen westartedourinvestigationinasitecoveringasurfaceof approx-imately1.5ha.Atthebeginningofourstudythetreeshadamean diameteratchestheightof7.79cmandameanheightof3.17m. Theywereplantedforrenaturatinganabandonedopen-pitcoal mine.
Foranalysingtheinfluenceofabioticfactorsonthepopulation dynamics,themeanairtemperature(◦C)andtheaccumulated pre-cipitation(mm)werechosen,asthesetwofactorsareknownto influencepsyllidpopulations(Hodkinson,2009).The meteorolog-icaldatawereobtainedfromameteorologicalstationsituatedat onekmfromthecentreoftheearpodtreeplantation.Asbiotic variables,wechosetheabundanceoffollowinggroupsof preda-torsandparasitoids(notidentified):Araneae,Coleoptera,Diptera, Formicidae,microhymenopteraandThysanoptera.
Spearman’scorrelation,suitablefordatawithnon-parametric distribution,wascalculatedusingthestatisticalprogrammeAction
Stat (Estatcamp, 2014), an extension programme installed in
MicrosoftOfficeExcel2010.
Results
Distributionandhostplants
We collected H. caldwelli in Brazil in the following three states: Minas Gerais, 1 female, Vazante, Fazenda Bainha, near source of Curtume river, S 17◦53.3/7 W 46◦55.2, 640–690m, 13–14.vii.2012,degradedCerradovegetation(DBurckhardtand DL Queiroz); 4 male, 7 female, same but Fazenda Bainha, S 17◦52.9/53.0W46◦53.0/55.1,660–670m,29–30.x.2012,E. contor-tisiliquum,Cerradovegetation,edgesofdisturbedforest,eucalypt plantation, creek;38 male, 32 female,47 immatures, samebut Fazenda Bainha, near source of Curtume river, S17◦53.3/7 W 46◦55.2,640–690m,11.ix.2014,degradedCerradovegetation;1 male,FazendaBocaina,S17◦53.6 W46◦54.7,642m,12.ix.2014, edgesofcerradoforest;1male,samebutVazante,S17◦58.1W 46◦54.3,723m,27.xii.2011,disturbedvegetationalongdirtroad; 54male,64f$,86immatures,samebutPatosdeMinas,Parque Mocambo,S18◦35.0/1W46◦30.3/4,830m,24.xii.2011,E. contor-tisiliquum,park;17male,13female,14immatures,1skin,same but11.vii.2012,Senegaliapolyphylla;1female,samebut27.x.2012, Libidibia ferrea. – Paraná, 2 male, 3 female,Ponta Grossa, Par-queEstadualdeVilaVelha,S25◦13.8–14.9W49◦59.5–50◦01.8, 860–900m, 17–18.ii.2016, E. contortisiliquum, Araucaria forest, transitionalforest,Baccharisscrub(DBurckhardtandDLQueiroz); 1female,same butColombo,Embrapacampus, S25◦19.2–20.1 W49◦09.4–10.1,920m,1–5.iv.2013,Albiziahassleri,remnantsof Atlanticforest,wasteplacewithBaccharisspp.,variousplantations; 1male,Curitiba,CentroPolitécnico,UFPR(UniversidadeFederaldo
292 L.M.Machadoetal./RevistaBrasileiradeEntomologia61(2017)290–293 1000 800 600 400 200 0 1 3 8 93 215 63 396 9 445462 Sampling dates Number of psylids May 2014
Jun Jul Aug Sep Oct Nov Dec
Jan 2015
Fev Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Jan 2016
Feb Mar Apr
T e mperature( °C) 884 9 29 4 0 22 4 525 151 519 153 30 293 14 0 5 10 15 20 25 30
Fig.2. PopulationdynamicsofHeteropsyllacaldwelli(bars)andmeanairtemperaturevariation(in◦C)inaseven-year-oldplantationofEnterolobiumcontortisiliquuminan
abandonedopen-pitcoalmineinCandiota,RS,betweenMay2014andApril2016.
1000 800 600 400 Sampling dates 0 2 4 6 8 10 Number of psylids Number of microhymenoptera 200 0 May 2014
Jun Jul Aug Sep Oct Nov Dec
Jan 2015
Fev Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Jan 2016
Feb Mar Apr
Fig.3. PopulationdynamicsofHeteropsyllacaldwelli(bars)andMicrohymenoptera(line)inaseven-year-oldplantationofEnterolobiumcontortisiliquuminanabandoned open-pitcoalmineinCandiota,RS,betweenMay2014andApril2016.
Paraná),S25◦26.8W49◦13.9,890m,4.i.2012,parkwithplanted trees,remnantsof Araucariaforest; 4 male,3female,same but 5–6.ii.2016,Albiziaedwallii;3female,samebutCuritiba,ParqueSão Lourenc¸o,S25◦23.1 W49◦15.9,940m,19.x.2012,Anadenanthera colubrina,plantedparkvegetation;1 female,samebutCuritiba, JardimBotânico,S25◦26.5W49◦14.3,910m,2.iv.2013, Anadenan-thera peregrina, planted park vegetation; 3 male, 1 female, 12 immatures,samebut Curitiba,ParqueBacacheri,S25◦19.2–20.1 W49◦09.4–10.1,920m, 17.i.2016,A. edwallii,park, remnantsof Atlantic forest. – Rio Grande do Sul, 4332 adults, Candiota,S 31◦33.3W53◦42.9,v.2014–iv.2016(LMMachado).
Populationdynamics
ForthestudiesonpopulationdynamicsinCandiota,we exam-inedatotalof4332adultH.caldwelli,2588inthefirst(59.7%)and 1744(40.3%)inthesecondyear.Inthefirstyear(May2014–April 2015),thepopulationpeakedinJanuary2015with884individuals collected.ThelowestnumberwasfoundinMay2014withonlyone sampledindividuals.Inthesecondyear(May2015–April2016),the populationpeakedinOctober2015with525individuals,thenin Decemberwith519.Thelowestvalueinthesecondyearwasfound inJulywithnospecimenrecorded.Thiswasthesoleperiodduring thetwoyearswherenoH.caldwelliwerefoundatall(Fig.2).
Therewasnorelationship betweenthe abundance distribu-tionsofthetwoevaluatedyears(0.43;p>0.05)withSpearman’s Correlationanalysis.For themeteorologicalvariables,therewas nosignificantcorrelationbetweenaccumulatedprecipitationand psyllidabundance(−0.013;p>0.05),buttherewasacorrelation betweenaverageairtemperatureandpsyllidabundance(0.658; p=0.0004)(Fig.2).Forthebioticfactors,therewasnosignificant correlationbetweentheabundanceofpredatorsandparasitoids andthatofH.caldwelli(p>0.05),withtheexceptionofthe microhy-menopterawherethecorrelationwassignificant(0.58;p=0.0027) (Fig.3).
The highest population number of microhymenoptera (884 psyllidsversusninemicrohymenoptera)wasinJanuary2015.In Octoberof2015,eightspecimensofmicrohymenopterawere sam-pled,coincidingwiththepopulationincreaseofH.caldwelli(Fig.3). Themoderatelysignificantcorrelationbetweenpsyllidsandtheir parasitoidsfoundinourstudymaybeduetothelowabundance ofbothpopulationswithvaluesnearorequaltozeroinMay,June, JulyandDecember2014andalsoinMay,JuneandJuly2015(Fig.3).
Discussion
ThespeciesH.caldwelliwasrecordedfromArgentina,Paraguay, Colombia,Panama,CostaRicaandNicaraguaassociatedwithAlbizia adenocephala(CostaRica,Panama)andE.cyclocarpum(Trinidad)
(Maesetal.,1993;Muddimanetal.,1992).ItsoccurrenceinBrazil
onE.contortisiliquum,whichwereporthereforthefirsttime,is thereforenotsurprising.Whetherthelargedistributionrangeof H.caldwelli is natural or a result of its widely plantedhost, E. contortisiliquum,isdifficulttoansweratpresent.Asforother psyl-lids,littleisknownaboutHeteropsyllainBrazil.Previouslyonly threespecies, viz.H.cubana,H.spinulosaandH.tenuata, possi-blyalsofromE.contortisiliquum,havebeenreportedfromBrazil
(BurckhardtandQueiroz,2012).
A.edwallii(Hoehne)BarnebyandJ.W.Grimes,E.contortisiliquum andS.polyphylla(DC.)Britton,allmimosoidFabaceae,arereported hereforthefirsttimeashostsofH.caldwellibasedontheimmatures foundontheseplants.Adultswerecollectedalsoontherelated speciesA.hassleri(Chodat)Burkart,A.colubrina(Vell.)BrenanandA. peregrina(L.)Speg.whicharelikelyhostsbutimmaturesareneeded toconfirmtheirhost-status(Burckhardtetal.,2014).Thisrelatively widehost-rangeaccordswithhostinformationonH.caldwelli pro-videdbyMuddimanetal.(1992),viz.AlbiziaadinocephalaandE. cyclocarpum,andisinlinewiththewidehostrangesofother Het-eropsyllaspecies(Muddimanetal.,1992).
FormostBrazilianpsyllids,littleisknownabouttheir popula-tiondynamics.ThefluctuationsofpopulationpeaksofH.caldwelli
L.M.Machadoetal./RevistaBrasileiradeEntomologia61(2017)290–293 293
duringthestudyperiodcanbeexplainedbythehighabundancein thefirstyearfromJanuarytoMarch2015(1791specimens=69.20% ofall specimens collectedinthefirst year). Thisis comparable toapopulationoutbreak,i.e.,ahighconcentrationofinsectsina shortperiodoftime(inourcase,threemonthsofthe12months evaluated).Inthesecondyear,therewasasuddenincreasein tem-peratureinAugust,precedingtheusualtimeoftemperaturerise, whichmayhavepromptedanearlyincreaseintheabundanceof psyllidsbeforetheusualperiodofoccurrence(summer).The popu-lationpeaksinthesecondyearoccurredinOctoberandDecember 2015,i.e.,earlierthanthatofthefirstyear.
GeigerandGutiérrez(2000)studyingtheecologyofH.cubana,
aspeciescloselyrelatedtoH.caldwelli,concludedthattheperiod betweenDecember andFebruaryisthemostfavourableforthe developmentofthispsyllid.Thiscoincideswithourobservations, particularlyforthefirstyearofcollection,whenfromDecember toFebruarytheabundancewith1338individuals(=51.70%ofthe yearlytotal)washighest.AccordingtoWalton(2003),the develop-mentofH.cubanaisbetterattemperaturesabove20◦C,whichis onlypartlyconsistentwithourresults:inJanuary2015,the popu-lationpeakoccurredwhentheaverageairtemperaturewasabove 20◦C,inthesecondyear,however,thepopulationpeakedthefirst timeinOctober2015,whentheaverageairtemperaturewasstill below20◦CandasecondtimeinDecember2015,withtheaverage airtemperatureabove20◦C(Fig.2).
ThepatternsofthepopulationfluctuationofH.caldwelliand themicrohymenopterainourstudyissimilartothatobservedby
FerreiraFilhoetal.(2008),whoalsoidentifiedpositivecorrelations
betweenthepopulationdistributionofthelerppsyllidGlycaspis brimblecombeiMooreandtheencyrtidPsyllaephagusbliteusRiek useditsthebiologicalcontrol.
Conclusions
TheoccurrenceofH.caldwelliinBrazilisnotsurprisingasithas beenreportedfromseveralneighbouringcountries.IntheSouth andSoutheastofBrazil,thespeciesiswidelydistributed.InBrazil, thepsyllid hasbeencollectedon A. edwallii,E.contortisiliquum andS.polyphylla,allpreviouslyunknownhosts.More collecting isrequired,particularlyinthenorth,toseeifH.caldwellidevelops inBrazilalsoonotherhostssuchasA.hassleri,A.colubrina,A. pere-grinaandE.cyclocarpum,onwhichadultswerecollectedorwhich arehostinothercountries.Moreworkisalsoneededtoseeifthe outbreaksofH.caldwelliarerelatedtophasesofflushofthehost andifthepresenceofthepsylliddamagesornegativelyinfluences itshost.
Conflictsofinterest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgments
We thank C.D. Aléné (Yaoundé, Cameroon) and an anony-mousreviewerforusefulcommentsandsuggestionsonaprevious manuscript draft. We are grateful to Capes (Coordenac¸ão de
Aperfeic¸oamento de Pessoal de Nível Superior) who provided financial support to the first author, and to the Companhia Riograndense de Minerac¸ão – Mina de Candiota and its staff for granting access to the study site and assistance and help during thefield work. We acknowledgethefollowing permits: IBAMA/SISBIO(11832—Licenc¸apermanenteparacoletadematerial zoológico;37053—Autorizac¸ãoparaatividadescomfinalidade cien-tífica:áreasforadeparquesemMG,PR,SCeRS)andCNPq(Projeto ‘BiodiversidadedePsylloideanoBrasil’,processodeExpedic¸ão Cientí-fican◦002152/2012).Thispaperispartofthedoctoralthesisofthe firstauthor.
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