Spatial distribution of Culicidae (Diptera) larvae, and its implications for Public Health, in five areas of the Atlantic Forest biome, State of São Paulo, Brazil

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REVISTA

BRASILEIRA

DE

Entomologia

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

Medical

and

Veterinary

Entomology

Spatial

distribution

of

Culicidae

(Diptera)

larvae,

and

its

implications

for

Public

Health,

in

ﬁve

areas

of

the

Atlantic

Forest

biome,

State

of

São

Paulo,

Brazil

Rafael

Piovezan

a,b,∗

_,

_João

_Paulo

_Oliveira

_Acorinthe

a

_,

_Jonas

_Henrique

_Teixeira

_de

_Souza

a

_,

Alexandre

Visockas

a

_,

_Thiago

_Salomão

_de

_Azevedo

c

_,

_Cláudio

_José

_Von

_Zuben

b

a_Prefeitura_Municipal,_Secretaria_Municipal_de_Meio_Ambiente,_Santa_Bárbara_d’Oeste,_SP,_Brazil

b_Universidade_Estadual_Paulista,_Departamento_de_Zoologia,_Rio_Claro,_SP,_Brazil

c_Universidade_de_São_Paulo,_Faculdade_de_Saúde_Pública,_São_Paulo,_SP,_Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received28July2016

Accepted29December2016

Availableonline6January2017

AssociateEditor:MariaAniceSallum

Keywords: Aedesaegypti Aedesalbopictus Dengue Entomologicalsurveillance Spatialanalysis

a

b

s

t

r

a

c

t

Inviewoftheadaptiveabilityofmosquitoesandtheirroleinthetransportofinfectiveagents, entomo-logicalsurveysundertakenintransitionalenvironmentsareveryimportantforthedeterminationofthe risktheyrepresentforPublicHealth.Amongtheprincipalvectorsoftheinfectiousagentsinvolvedin theoccurrenceofimportantarboviruses,suchasdengue,forexample,aretheCulicidae-insectscapable ofinstallingthemselvesintheurbannuclei,whichexistwithinareascontainingvestigialforests.This presentstudyconductedasurveyofmosquitospeciesbymeansoftrapstocatchtheirlarvaeinstalled infiveruralareaswithintheAtlanticForestdomainandcontainingitsvestigialvegetationinthe munic-ipalityofSantaBárbaraD’Oeste,SãoPaulo,Brazil.Atotalof13,241larvaebelongingtosixmosquito specieswerecollectedon920occasions(32.52%ofpositivecollections).Aedesalbopictus(64.23%)and Aedesaegypti(32.75%)werethemostfrequent,followedbyCulexquinquefasciatus(1.32%),Aedes fluvi-atilis(1.04%),CulexComplexCoronator(0.40%)andToxorhynchitestheobaldi(0.22%).Threeareaswere analyzedbymeansofSimpson’sdiversityindexandthespatialanalysisshowedthatthesiteswiththe greatestabundanceofAe.aegyptipresentedlowerdiversityvaluesandwereassociatedwithmorehighly consolidatedurbannuclei.Thevectorofdengue,chikungunyaandzikahasgreatinfestingabilityinurban areas,whichmeansthattheearlyimplementationofentomologicalsurveillanceandcontrolactivities inspecificareas–suchastransitionalones–ishighlyimportant.

Introduction

Somemosquitospeciestransmitpathogensandcontributeto

thedisseminationof diseasearoundtheWorld(Marcondesand

Ximenes,2015).InBrazil,thecontrolofdiseasessuchasdengue, chikungunyaandzika,allofthemarbovirusestransmittedbythe samecommonvector,standsoutasoneofthegreatestinvestments inthePublicHealthﬁeldinthecountry,giventheseriousnessand theimpactofthesediseasesonsociety(Câmaraetal.,2007;Brazil, 2015).ThismakesthesurveillanceofCulicidaevectorspecies

dis-persal and dynamics in both endemic and non-endemic areas

extremelyimportant.

∗ Correspondingauthor.

E-mail:piovezan.rafael@gmail.com(R.Piovezan).

TheCulicidaefamilyissubdividedintoAnophelinaeand Culic-inae.Thislattergroupisthelarger,consistingofmorethan3500 species,108generaand11tribes.AmongtheCulicidaearespecies

whose representatives are of great epidemiological importance

(ConsoliandLourenc¸o-de-Oliveira,1994;Harbach,2016).

Ecological dynamic and the relations established between

mosquitospeciesarethusseentobeimportantformedical

ento-mology,especiallyunderconditionsoftransitionbetweenurban

andruralenvironments.In theselocalities,interspeciﬁc compe-titionandenvironmentalfactorsmayalterthedominanceofone speciesoverothers(Julianoetal.,2002),creatingconditions appro-priateforthetransmissionofpathogensandconsequently,forthe occurrenceofdiseaseoutbreaksandepidemicsinthehuman pop-ulationestablishedintheseareas.

Thesetransitionalenvironments,asoneisnotheredealingwith

consolidated urbanareas,may not bebeneﬁted byvector

con-trolactivitiesinthesamewayaswhenthesearecarriedouton

http://dx.doi.org/10.1016/j.rbe.2016.12.007

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theoutskirtsofcities.Withinthiscontext,entomological surveil-lanceisofthegreatestimportance–andamongthemostefﬁcient andsensitivemethodsformonitoringmosquitoesareovitrapsand larvitraps,bothofwhicharewidelyused(BragaandValle,2007; Brazil,2009;Silvaetal.,2009;SUCEN,2010),beingofextremely simpleapplicationfor usein thedailyroutineofentomological surveillance.

Entomologicalsurveillanceisthereforeanimportanttoolinthe accompanimentofthemosquitopopulationsfoundinruralareas, seeingthatitassistsinexpandingknowledgeofthepatternsof occupationandpermitsthedevelopmentofstrategiesofcontrol addressedtothespeciﬁcspecies.Further,theinterpolationofthe

mosquitodiversitypresentedonthemapsproducedpermitsthe

differentiationofthediversityexistinginthedifferentregionsof eachoftheareasandtheestimationofthevaluesintheareasin whichcollectionshavenotbeenundertaken.

OurstudyseekstopresenttheCulicidaefaunafoundin differ-entruralareasof themunicipalityof SantaBárbarad’Oeste, as

alsothecompositionof thespeciesin theseplacesbymean of

theuseoflarvitraps.Theplacesselectedarethelargest popula-tionnucleifoundoutsidetheurbancenter,andraisethepossibility

oftheseenvironments’presenting casesof diseaseswhich

nor-mallycirculateintheurbanareasandwhoseetiologicalagentsare mosquito-borne.Undertheseconditions,itisimperativeto under-takeamorerigorousanalysisofcontrolactions,whichinvariably requireadaptationssothattheymaybecarriedoutintransitional environments–asisthecaseoftheruralareas.Therealsoemerges thefurtherpossibilityofthedispersalofpathogenswiththe partic-ipationofmosquitoes,involvingbothforestedenvironmentsand urbanareas.Thisisanimportantcondition,seeingthatthere is considerablemovementofpeopleintheseplaceswhichoften con-tainspeciﬁcstructuressuchasschools,churchesandhealthposts, amongothers,knowntobecentersforsocialgatherings.

Materialandmethods

ThispresentstudywasundertakeninthemunicipalityofSanta Bárbarad’Oeste,situatedintheinteriorofSãoPaulostate(Fig.1), at22.75◦Sand49.38◦W,withanaveragealtitudeof560m.The totalareaofthemunicipalityisofapproximately271km2_,_with

apopulationestimatedatabout190thousandinhabitants,98%of

whomareconcentratedintheurbanareaandjust2%ofwhom

livein theruralzone(IBGE,2013).Themunicipalityis situated amongthefoothillsoftheDepressãoPeriféricaPaulista, possess-ingreliefofgentlyundulating,medium-sizedhills.Thesurviving vegetationoftheareabelongstoazoneoftransitionbetweenthe AtlanticForestandSavannahbiomes.Inaccordancewiththe

clas-siﬁcationproposedbyKoeppen,SantaBárbarad’Oestepossesses

aclimatedeﬁnedasCwa,characterizedastropicalhighlandwith summerrainfallanddrywinters.Theaveragetemperatureofthe hottestmonthisabove22◦Candthatofthecoldestmonth12◦C. Theaverageannualrainfallisof1466mm(IBGE,2013;CEPAGRI, 2014).

Thesampleswerecollectedbymeansoflarvitrapsduringthe periodfromFebruary2013toMarch2014,inclusive,givingatotal of14monthsofcollections.Fiveruralareasofthemunicipality wereselected(Fig.1),namelythesuburbsofCruzeirodoSul,Vale dasCigarras,SantaAlice,SantoAntôniodoSapezeiroandGlebas Califórnia.Thetrapsweredistributedinthesuburbscited,usingas criterionaratioofonetrapper90inhabitants.Theseplaceswere selectedbecausetheyarethelargestresidentialnucleioutsidethe urbanperimeterofthemunicipality.It isimportanttoaddthat eachoftheseareaspresentsitsownspeciﬁccharacteristicsinterms ofscenerystructure,beingmoreorlessclosetoforestfragments andpresentingdifferencesastotheproximityofrivers,thesizeof

theresidentpopulationandtheurbanstructuresinstalled(schools, churches,healthposts).

Thetotalnumberoftrapsineachsuburbwasthusasfollows:

Cruzeirodo Sul– 13; Valedas Cigarras – 12;Santa Alice – 9;

SantoAntôniodoSapezeiroandGlebasCalifórnia –2each.The

blockswereselectedandthehousesdrawnbylotvisitedtorequest permissionfortheinstallationofthetraps,thusgivingatotalof thirty-eightlarvitraps,whichwereinspectedweeklythroughout thestudyperiod.

Thelarvitraps,consistingoftirescuttransversely,wereﬁxed intheperidomicileofthesitesselected.Afteritsinstallation,each trapreceivedapproximately1Lofwaterandremainedinthesame placeforthesubsequentweeklyinspections.Duringthe

inspec-tions, themosthighlydeveloped larvaewerecollectedandthe

liquidfromthetrapwasfilteredforthecollectionoftheremaining larvaewhichwere,later,transferredtoplasticrecipients.The lar-vaewereindividuallyidentifiedinthelaboratorywiththehelpofa microscopeandtheuseofdichotomicidentificationkeys(Consoli andLourenço-de-Oliveira,1994;Forattini,2002).

Theresultswerestoredinaspatialdatabankwhichpermitted theveriﬁcationofthespatialdistributionoftheCulicidaespeciesin theruralareaofSantaBárbarad’Oestestudied.However,samples fromSantoAntôniodoSapezeiroandGlebasCalifórniawere omit-tedfromthisanalysisastheydidnotpresentsigniﬁcantsampling units.

SpatialanalysisofCulicidaedistribution

Thegeo-referenced sitesof thetrapswere transformedinto

aspatialinformation planeina GeographicInformationSystem

(ArcViewTM₎₍_EsriTM_,₁₉₉₆_),_into_which_were_entered_data_on_the

positivityofthemosquitospecies.Theconnectionbetweenthe geo-graphicalcharacteristicsandthetableofattributesisguaranteedby thegeo-relationalmodel,thatistosay,onesingleidentiﬁer under-takestheconnectionbetweenthem,maintainingacorrespondence

between the space and the register of attributes. The table of

attributes was provided with the occurrences of the mosquito

speciesclassiﬁedinhierarchiesinthefollowingtwoforms:total

numberofspeciesandnumberofco-habitations.Thisprocedure

permitsthecompilingofsixthememaps,onwhichtheplaceswith thegreatestmosquitofrequencywereidentiﬁed.

SpatialanalysisofCulicidaediversity

To undertake this spatial analysis, the diversity indices of

ShannonandSimpsonwereﬁrstestimatedforeachofthetraps

distributedintheCruzeirodoSuldistrictofthecityofSanta Bár-barad’Oeste.Theproceduresemployedtocalculatetheseindices aredescribedinMagurran(1988).

Afterestimatingtheseparameters,ananalysiswasundertaken onthebasis ofthecollectionofsemi-variogramsofthespecies diversity,becausethisistheﬁrstandmostimportantphaseseeing thatthistypeofapproachanalyzesthespatialdependenceofthe valuesofavariableV(x),separatedbyavectorh.

Andriotti(2004)deﬁned thesemi-variogramas thevariance

of theerrorcommitted by theestimation of anunknown

con-tentin(x+h)withthehelpofaparticularpointin(x),thatisto say,semi-variogramsexpressthespatialdistributionofa continu-ousvariable,showingitszoneofinﬂuenceandanisotropicaspects, implyingapreferentialdirectionforthespatialdistributionofthe variable(Pfeifferetal.,2008)andthepresenceofanomaliescaused

bysamplingerrororrandomcomponents.

Semi-variogramsofthediversityofmosquitospecieswere

esti-matedinordertoobtainamathematicalmodelformountingthe

variabilityofallthedata.Thevariogramisanimportanttoolwhich demonstratesthedegreeofspatialdependenceofthesampleand

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Cruzeiro do Sul

Vale das Cigarras

Glebas Califórnia N E 4º 0º 4º 8º 12º 16º 20º 24º 28º 32º 20º 25º 45º 52º Study Areas Santo Antônio Sapezeiro Santa Alice Biome Savanna Atlantic forest Traps 30º 42º 54º 66º S W

Fig.1. LocalizationofthestudyareasintheAtlanticForestbiome,SãoPaulostate–Brazil.

itsspecificsupport.Therelationisexpressedontwoaxes,xwhich expressesthevectorofthedistanceandywhichisdenominated varianceorcovariance.Inthispresentstudy,thesemi-variograms assistintheverificationoftheexistenceofthelackofspatial corre-lationandcontributetothevalidationoftheexperimentalmodelof collection,inviewofthefactthatthesiteswerechosenrandomly andthefindingofthelarvaeandthespecieswasfortuitous(Isaaks andSrivastava,1989).

Ordinarykrigingwas,therefore,adoptedasthemethodof

inter-polationfor the compiling of maps of mosquito diversity. This

procedurewasundertakenonsurfersoftware(GoldenSoftware,

1995)and resultedin theconstructionof fourquantitative iso-pleticmaps.Thismapconsistsoflinesthatlinksitesofdiversity distributionshowingthespatialdistributionandabundanceofthe Culicidaespecies.

Results

Duringtheperiodofthestudy,Culicidaelarvaewerecollected on920occasions(32.52%ofpositivecollections),719withoutthe larvaeofotherspeciesand201jointlywithothers (therebeing

more than one species present in the trap at the moment of

collection).Takingallthecollectionsmadeintoconsideration,a totalof 13,241larvaewereidentiﬁed inthelaboratory, belong-ingtosix differentspecies:Aedes (Stegomyia) albopictus‘Skuse,

1894(1895):20(F*;Culex)’,Aedes (Stegomyia)aegypti ‘Linnaeus, 1762:470(A;Culex)’,Aedes(Georgecraigius)ﬂuviatilis‘Lutz,1904:72 (A;asCulex)’,Toxorhynchites(Lynchiella)theobaldi‘DyarandKnab,

1906c:246(M.F;Megarhinus)’,CulexCoronatorComplexandCulex

(Culex)quinquefasciatus‘Say,1823:10(A;assp.)’.Thespeciesand

thepercentagesof each ofthem,whetherfoundin isolationor

jointlywithothers,arepresentedinTables1and2.

The occurrences when there were more than one species

present were dominated by Ae. albopictus and Ae. aegypti, in

absolute values, which were present in 77.61% of the catches.

Thiskindofoccurrencewasdistributedbyareaasfollows:106

in Cruzeirodo Sul, 46 in Vale das Cigarras, 38 in SantaAlice,

9 in Glebas Califórnia and one in Santo Antônio do Sapezeiro

(Table 2).As hasalready been cited, the species Ae. albopictus and Ae.aegypti presented thegreatest absolutevalues interms ofco-habitation,thougha proportionalanalysis–thatistosay, thenumberofoccurrencesofthespeciesincohabitationin rela-tiontothetotal numberof occurrencesofthat samespeciesin thearea–demonstratedthatAe.albopictusandAe.ﬂuviatiliswere thespecieswhichpresentedthehighestproportionalvalues,being, inCruzeirodoSul6.8%andinValedasCigarras11.3%.Thusalso Tx.theobaldipresentedhighproportionalvalues,cohabiting42.8% ofthetimesinwhichthespeciesappearedinValedasCigarras,

in 50%inSantaAlice andin 100%of theoccurrencesinGlebas

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Table1

SpeciesofCulicidaecollectedinlarvitrapsintheruralareasofthemunicipalityofSantaBárbarad’OestefromFebruary2013toMarch2014.

Species CruzeirodoSul ValedasCigarras SantaAlice Sto.A.Sapezeiro GlebasCalifórnia Allﬁveareas NLarvae %Larvae NLarvae %Larvae NLarvae %Larvae NLarvae %Larvae NLarvae %Larvae Ntotal %Total

Ae.aegypti 1945 42.01% 479 14.63% 1787 48.53% 56 26.67% 70 4.84% 4337 32.75% Ae.albopictus 2533 54.72% 2676 81.73% 1865 50.65% 118 56.19% 1313 90.8% 8505 64.23% Ae.ﬂuviatilis 44 0.95% 53 1.62% 28 0.76% 14 6.67% – – 139 1.05% Cx.quinquefasciatus 56 1.21% 37 1.13% – – 22 10.48% 61 4.22% 176 1.33% Cx.CoronatorComplex 39 0.84% 15 0.46% – – – – – – 54 0.41% Toxorrynchitestheobaldi 12 0.26% 14 0.43% 2 0.05% – – 2 0.14% 30 0.23% Total 4629 100% 3274 100% 3682 100% 210 100% 1446 100% 13,241 100%

N,representsthenumberoflarvaefoundinthecollections.

Ae.albopictuswasthespeciesmostfrequentlyfoundduringthe studyandrepresented95.5%oftheoccasionswhenitwasfound jointlywithother speciesand 67.68% when caughtin isolation (withjust onespeciespresentduringthecollection).Ingeneral, takingbothsituationsintoconsideration,thelarvaeofthisspecies accountedfor64.23%ofthetotalfound.

For Ae. aegypti, the second most abundant and frequent in thisstudy,itsdistributionbyareawaspatchy.The highest val-uesobtained,intermsoftheproportionoflarvaeofthisspecies foundinrelationtothetotalnumber,wereobservedinCruzeirodo SulandSantaAlice(Table1).Theoccasionsonwhichtwoormore specieswerefoundtogetherwerealsomorefrequentinthosetwo districts(Table2).

Theotherspecies of Culicidaepresented a low frequency in

theareasstudied.Culexquinquefasciatuswasthethirdmost abun-dant,followed by Ae. ﬂuviatilis,Cx. Coronator Complexand Tx. theobaldi.ThespatialdistributionofCulicidaespeciesinthe dis-trictsofCruzeirodoSul,ValedasCigarrasandSantaAliceisgiven inFigs.2–4.ThesmallnumberofsamplesfromtheareasofSanto AntôniodoSapezeiroandGlebasCalifórniamadeitimpossibleto mapthedistributionofthespeciesthereandtheseareashavenot thereforebeenincludedinthegraphicrepresentationsofthe cal-culationsofdiversity.

Thevariographicanalysisof Simpson’sandShannon’s

diver-sity indices may be seen in Fig. 5. Shannon’s index shows a

very clearly fragmented effect which reveals a lack of spatial

correlation with the variable studied, whereas for Simpson’s

indexthis effectissmaller.Theseresultsshowthat thekriging methodofinterpolationmayonlybeappliedtoSimpson’sdiversity index.

On the basis of these ﬁndings, the experimental

semi-variograms of Shannon’s diversity index for theCruzeiro, Vale

das Cigarras and Santa Alice rural districts were rejected and

replacedbytheexperimentalsemi-variogramsofSimpson’s diver-sityindexforthesamelocalities.Theappropriate experimental semi-variogramsweretakenintoconsiderationandtheadjustment tothetheoreticalmodelundertaken.Theresultsoftheadjustment (Fig.6)showthatthemostappropriatemodelisthelinearone.In thesemodelstheinclinationstakeonavaluewhichapproximates to6.5andattaintheirhighestlevel(C)at3.086,2.729and0.0032, themaximumdistancewithinthemosquitoisspatially autocorre-latedare730m,64mand620mrespectively,fortheruraldistricts ofCruzeirodoSul,SantaAliceandValedasCigarras.This

corre-spondsinpracticetoadistanceatwhichthe95%thresholdwas

attained.

Afterthedevelopmentoftheexperimentalsemi-variogram,the estimationofthespatialdistributionofSimpson’sdiversityindex (Fig.7)forthethreesuburbswasundertaken.Thisﬁgureshowsthat thecentralandnorthwesternareasoftheSantaAliceruraldistrict presentthegreatestmosquitodiversity(0.96).Thesouthernpart ofthisruraldistrictpresentsthesmallestdiversity(0.42).

ThediversitymapfortheruraldistrictofCruzeirodoSulshowed thatthediversityisgreater(between0.78and0.86)initswestern andsoutheasternparts.IntherestofthisruraldistrictSimpson’s diversityattainsitssmallestmagnitude(0.42).

Finally,intheValedasCigarrasruraldistrict,thediversityis greatestinthesouthernpart(0.86),thoughitismoreevenly dis-tributedthanintheotherruraldistricts.Inthisareaoneﬁndsthe regionswiththeleastdiversitysituatedinthenortheasternand westernparts.

Table2

SpeciesofCulicidaecollectedinlarvitrapstogetherwithotherspecies(cohabitation)intheruralareasofthemunicipalityofSantaBárbarad’OestefromFebruary2013to

March2014.

Speciescollectedtogether CruzeirodoSul ValedasCigarras SantaAlice Sto.A.Sapezeiro GlebasCalifórnia Allﬁveareas

N % N % N % N % N % N %

Ae.aegyptiXAe.albopictus 95 89.62% 22 47.82% 34 89.47% 1 100% 4 44.45% 156 77.61%

Ae.albopictusXAe.ﬂuviatilis 3 2.83% 6 13.04% – – – – – – 9 4.47%

Cx.quinquefasciatusXAe.albopictus 1 0.94% 1 2.17% – – – – 2 22.23% 4 1.99%

Cx.CoronatorComplexXAe.aegypti 1 0.94% – – – – – – – – 1 0.49%

Cx.CoronatorComplexXAe.ﬂuviatilis – – 1 2.17% – – – – – – 1 0.49%

Ae.albopictusXToxorrynchitestheobaldi 2 1.88% 6 13.04% – – – – 2 22.23% 10 4.97%

Cx.quinquefasciatusXAe.aegypti – – 2 4.34% – – – – – – 2 0.99%

Ae.aegyptiXToxorrynchitestheobaldi – – – – 1 2.63% – – – – 1 0.49%

Cx.CoronatorComplexXAe.albopictus 1 0.94% 2 4.34% – – – – – – 3 1.49%

Ae.aegyptiXAe.albopictusX Toxorrynchitestheobaldi

2 1.88% 1 2.17% – – – – – – 3 1.49%

Ae.aegyptiXAe.albopictusXAe. ﬂuviatilis

1 0.94% 6 13.04% 3 7.89% – – – – 10 4.97%

Cx.quinquefasciatusXAe.albopictusX Ae.aegypti

– – – – – – – – 1 11.12% 1 0.49%

Total 106 100% 47 100% 38 100% 1 100% 9 100% 201 100%

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Aedes albopictus

Aedes aegypti

Culex quinquefasciatus

Aedes fluviatilis

Culex

coronator complex

Toxorhynchites theobaldi

7 484 400 7 484 000 7 483 600 7 483 200 7 482 800 243 800 244 200 244 600 245 000 245 400 7 484 400 7 484 000 7 483 600 7 483 200 7 482 800 243 800 244 200 244 600 245 000 245 400 7 484 400 7 484 000 7 483 600 7 483 200 7 482 800 243 800 244 200 244 600 245 000 245 400 7 484 400 7 484 000 7 483 600 7 483 200 7 482 800 243 800 244 200 244 600 245 000 245 400 7 484 400 7 484 000 7 483 600 7 483 200 7 482 800 243 800 244 200 244 600

Legend

Number of individuals +501 N W E Santa Bárbara d’Oeste Municipality SP - BRA Study Area S 0 143 286m 351 a 500 201 a 350 51 a 200 1 a 50 245 000 245 400 7 484 400 7 484 000 7 483 600 7 483 200 7 482 800 243 800 244 200 244 600 245 000 245 400

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7 482 600 7 482 200 7 481 800 245 800 246 200 246 600 7 482 600 7 482 200 7 481 800 245 800 246 200 246 600 7 482 600 7 482 200 7 481 800 245 800 246 200 246 600 7 482 600 7 482 200 7 481 800 245 800 246 200 246 600 7 482 600 7 482 200 7 481 800 245 800 246 200 246 600 7 482 600 7 482 200 7 481 800 245 800 246 200 246 600

Aedes albopictus

Aedes aegypti

Culex quinquefasciatus

Aedes fluviatilis

Culex

coronator complex

Legend

Number of individuals +501 301 a 500 N E S 0 143 286 Santa Bárbara d’Oeste Municipality SP - BRA Study Area m W 201 a 350 51 a 200 1 a 50

Toxorhynchites theobaldi

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7 479 400 7 479 200 7 479 000 7 478 800 7 478 600 252 700 252 900 253 100 253 300 253 500 7 479 400 7 479 200 7 479 000 7 478 800 7 478 600 252 700 252 900 253 100 253 300 253 500 7 479 400 7 479 200 7 479 000 7 478 800 7 478 600 252 700 252 900253 100 253 300253 500 7 479 400 7 479 200 7 479 000 7 478 800 7 478 600 252 700252 900253 100 253 300253 500 7 479 400 7 479 200 7 479 000 7 478 800 7 478 600 252 700 252 900253 100

Legend

Number of individuals +501 351 a 500 201 a 350 51 a 200 1 a 50 0 143 286m Santa Bárbara d’Oeste Municipality SP - BRA Study Area

Toxorhynchites theobaldi

Culex

coronator complex

Aedes fluviatilis

Culex quinquefasciatus

Aedes aegypti

Aedes albopictus

S N E W 253 300253 500 7 479 400 7 479 200 7 479 000 7 478 800 7 478 600 252 700252 900253 100 253 300253 500

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0.081 0.072 0.063 0.054 0.045 0.036 0.027 0.018 0.009 0.16 0.14 0.12 0.10 0.08 0.06 0.04 0.02 0 0.16 0.14 0.12 0.10 0.08 0.06 0.04 0.02 0 0 100 200 300 400 500

Shannon diversity omnidirectional Shannon diversity omnidirectional Shannon diversity omnidirectional

Cruzeiro do Sul

Santa Alice

Cigarras

Simpson diversity omnidirectional Simpson diversity omnidirectional Simpson diversity omnidirectional

600 700 800 0 0.005 0.010 0.015 0.020 0.025 0.030 0.035 0.040 0 100 200 300 400 12 18 30 40 20 20 16 24 22 8 16 24 22 22 72 54 8 8 16 34 24 18 500 600 700 800 0 60 120 180 240 300 360 420 480 540 0 0.004 0.008 0.012 0.016 0.020 0.024 0.028 0.032 0 60 120 180 240 300 360 420 480 540 0 0 8 54 72 22 C(0)–C(h) C(0)–C(h) C(0)–C(h) C(0)–C(h) C(0)–C(h) C(0)–C(h) 200 400 600 800 1000 0.0054 0.0064 0.0056 0.0048 0.0040 0.0032 0.0024 0.0016 0.0008 0 0 200 400 600 800 1000 1200 1200 (h) (h) (h) (h) (h) (h)

Fig.5.Semi-variogramsofShannonandSimpsondiversityindices.

Discussion

Larvitraps employed in this present study resulted in the collection of a total of 13,241 larvae of six distinct Culicidae species. Despite their simplicity, larvitraps can give satisfac-toryresults, permittingthemonitoringof species thehabits of developmentofwhoseimmaturestagesinvolvetheuseofboth naturalandartiﬁcialbreedingplaces(SUCEN,2001;Brazil,2002; Gama et al., 2007; Alarcón-Elbal et al., 2014; Monteiro et al., 2014a,b), as they also demonstrate the ecological plasticity of

thespecies found and theirpotential for adaptation tohuman

dwellings(Lopes,1997),makinguseofartiﬁcialbreedingplaces

for the development of their immature forms. Both breeding

places and traps made from tires have already demonstrated

theirefﬁciencyinsurveysundertakennearurbanareasor even

indegradedforestareas(Lopesetal.,1993),which haveshown

themselves to be similar to those investigated in this present

study.

ThedistributionofAe. albopictusin thevarious areasof col-lectionwasseentobeuneven.Itwasthemostabundantspecies, attainingthegreatestvalue(90%frequency)ofallthelarvae sam-pledinGlebasCalifórnia.SpeciﬁcallyintheareaofCruzeirodoSul,

Piovezanetal.(2013)hadalreadyobservedthedistributionofthis species,andthecomparisonofthesetwostudies,undertakenin thesameareawithanintervaloftwoyearsbetweenthem,showed areductioninthepercentagesoftheoccurrenceofAe.albopictus andanincreaseobservedforAe.aegypti.Although,inBrazil,Ae. albopictushasnotbeenincriminated inthetransmissionofthe

Denguevirus, it possesses theproven competenceof

transmit-tingseveralarbovirusessuchasDengueandChikungunya(Gratz, 2004;MarcondesandXimenes,2015).Further,asregardsdengue, thisvector’sabilityhasbeenprovedbytheepidemicsthathave occurredinJapan,Indonesia,theSeychelles,ThailandandMalaysia (Gratz,2004),inHawaii(Efﬂeretal.,2005),Gabon(Paupyetal., 2010)andinEurope(Fieldetal.,2010;LaRucheetal.,2010).The ChikungunyavirushasalsobeentransmittedbyAe.albopictus,as

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Cruzeiro do Sul

Santa Alice

Cigarras

Variography parameters

C (Sill) Co (Nugget) A (Range) C(0)–C(h) (Distance) Anisotropic 3.2×10-3 0.015 620 0.15 1.00

Variography parameters

C (Sill) Co (Nugget) A (Range) C(0)–C(h) (Distance) Anisotropic 2729 0.002 640 0.031 1.8

Variography parameters

C (Sill) Co (Nugget) A (Range) C(0)–C(h) (Distance) Anisotropic 3086 0.0014 730 0.0032 0.23 0.0054 0.0064 0.0056 0.0048 0.0040 0.0032 0.0024 0.0016 0.0008 0 0 0 0.004 0.008 0.012 0.016 0.020 0.024 0.028 0.032 0 0 0.005 0.010 0.015 0.020 0.025 0.030 0.035 0.040 0 100 200 300 400 12 16 34 24 18 500

Simpson diversity omnidirectional Simpson diversity omnidirectional Simpson diversity omnidirectional

(h) (h) (h) C(0)–C(h) C(0)–C(h) C(0)–C(h) 600 700 800 60 120 180 240 16 24 22 8 300 360 420 480 540 200 400 8 54 72 22 600 800 1000 1200

Fig.6.AdjustedSemi-variogramsoftheSimpsondiversityindex.

hasrecentlybeenreportedinEurope,AfricaandtheIndianOcean (Reiteretal.,2006;Bonilaurietal.,2008;Pagèsetal.,2009;Paupy etal.,2010).

Aedesaegyptiwasthesecondmostfrequentspeciesoverall, pre-sentingpatternsofoccurrencewhichvariedbetween5%inGlebas Califórniaand49%inSantaAlice.Thisspeciespresentsahighdegree

ofanthropophilyandhasspreadintourbanareasbymakinguse

ofartificialbreedingplacesassitesforreproduction(Consoliand Lourenço-de-Oliveira,1994).Ontheotherhand,itspresencein rel-ativelywellvegetatedareasisduetoitsecologicalplasticityinthe colonizationofhabitats,anditsabilitytodevelopinnatural breed-ingplacessuchasthoseprovided bybromeliads(Souza-Santos, 1999;ForattiniandMarques,2000;Varejãoetal.,2005;Gonçalves andMessias,2008).Ashasbeenstatedabove,significantchanges initsabundancewereobservedintheCruzeirodoSulareaas com-paredwiththeresultspreviouslyobtainedbyPiovezanetal.(2013). Thisspeciesincreasedfrom8.1%ofthesamplesobtainedinthatfirst studytothe42%observedinthisone,thuspresentinganincrease

inthespecies’frequencyandindicatingapossiblereplacementof Ae.albopictus.

TheinteractionbetweenAe.aegyptiandAe.albopictusmaybe inﬂuencedbyenvironmentalfactors.Insituationsofco-habitation, thecharacteristicsofthesceneryand environmentalconditions maybedeterminingfactorsinthesuccessorfailureofthespecies. Placeswithaccentuatedruralcharacteristicsandthepresenceof vegetationfavorthedisplacementandexclusionofAe.aegyptiby

Ae. albopictus,while inurban environmentsorthose subject to

greatanthropicinﬂuence,Ae.aegyptipersistsordominatesoverAe. albopictus(Lounibosetal.,2010).Insituationsinwhichthequantity offoodavailableisreducedorevenslightlylimited,theinterspeciﬁc

larvalcompetitionisthemainfactordeterminingtheabundance

ofthesetwomosquitospeciesanditisAe.albopictuswhich,under thesecircumstances,hastheadvantageoverAe.aegypti(Braksetal., 2004).However,underenvironmentalconditionssuchasthelow

relative humidityand hightemperatureswhich prevailin drier

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Santa Alice Cigarras 0 80 160 m 0 7 479 300 7 479 100 7 478 900 7 478 700 7 484 400 7 483 600 7 482 800 243 800 244 600 245 400 252 700 0 130 260 m Cruzeiro 253 000 253 400 245 800 7 481 800 7 482 200 7 482 600 246 200 Legend N W E S

Santa Bárbara d’Oeste City

0.42 0.56 0.66 0.76 0.86 0.96

246 600

125 250 m

Fig.7. Simpsondiversityindexmaps.

seeingthatAe.albopictusismoresensitivetothesevariations,both intheeggandintheadultphases(Julianoetal.,2002).

Ae.aegyptiandAe.albopictuswerealsothosewhichwerepresent ingreaternumbersinsituationsofcohabitation,onatotalof156 occasions.InCruzeirodoSul,ofthetotaloftheirjointoccurrencesin thearea,89.62%wereofthesetwospecies.Themethodofcollection employinglarvitrapsiswidelyusedinmonitoringresearchprojects relatedtothesetwospecies,whichexplainsthegreaterfrequency withwhichthesetaxawerefoundinthisstudy.Theanalysisofthe ﬁguresgeneratedshowsthatthespatialdispersionofAe.albopictus hasalwaysbeenmorecloselyassociatedwithareasclosetodenser vegetationcoverorbodiesofwater.

Further,relating totheoccurrencesin co-habitation,in rela-tiveterms,thatistosay,comparingthenumberofoccasionson

whichthespecies appearsinco-habitation withthenumber of

totaloccurrencesofthespeciesin aparticulararea,Ae. albopic-tusand Ae. fluviatilispresented highervalues. The stratification intheforagingofthespeciesmightbeoneofthefactorswhich influencecoexistenceinenvironmentssuchasthebreedingplaces,

beyondwhichoneshouldtakeintoconsiderationthatthereexist

variousecologicalrelationshipswhich presentadependence on

environmentalfactors,densityofexistingpopulations,presenceof predatoryspecies,oreventhekindoforganicmaterialusedtofeed thelarvae(Juliano,2009).

For Ae. aegypti, the places in which the species had its

densest distribution were closer to the more urban stretches

of theareas concerned, demonstrating the needto accompany

the density of this mosquito species in transitional areas with

ruralcharacteristics butclose tourbannuclei – whether

exist-ing or in process of development. Its epidemiological role in

the transmission of pathogens on several of the continents

(Consoli andLourenc¸o-de-Oliveira,1994)causesgreatproblems

within the ﬁeld of Public Health and considerable economic

loss in terms of the attendance to and treatment of patients

(Kouri et al., 1981). The present Zika virus epidemic in Brazil and itsconsequences constitutea factor ofthe greatest

impor-tance which has to be taken into consideration especially in

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areas.

Thevectorcontrolactivitiesforeseenforurbanareasarenot normallyextendedtocovertransitionalareassuchas,for exam-ple,ruralareas,asthepresence ofAe. aegypti inthese latteris lessfrequent.Oneshouldalsobearinmindthedifferencebetween thebreedingplacesoftenavailable,whicharedistinctasbetween urbanareasandruralenvironments.Theanalysisofthesceneryalso takesimportantdifferencesintoconsideration,therebeing impor-tantdifferencessuchasthegreaterdensityoftreesinruralareas, whichmakescontrolbynebulization,forexample,difﬁcult,and

theenvironmentalimpactonwildarthropodswhicharenotthe

targetofcontrolprogramsandarefrequentlyfoundintransitional environments.

TheincreaseintheabundanceofAe.aegyptiinCruzeirodoSul, evidentwhenthepresentstudyiscomparedwiththatofPiovezan etal.(2013),mayberelatedtothefactthatthisspecies’eggsare moreresistanttodesiccationandtolongperiodsofdroughtthan arethoseofAe.albopictus(Julianoetal.,2002).Thishypothesisis basedonthefactthatthisregionfaced,intheyears2013and2014, theperiodinwhichthispresentstudywascarriedout,thelongest dryperiodinallofrecenthistory,withavolumeofrainfallbelow theaverageofthelast50years(Coelhoetal.,2015,2016),which wouldgiveacertainadvantagetoAe.aegypti,tothedetrimentof Ae.albopictus.

Ae. aegypti hasdominated urban environments and

demon-stratedgreatadaptabilityinitsuseofbreedingplaces(Forattini, 1992;ConsoliandLourenc¸o-de-Oliveira,1994;Barataetal.,2001). Thecontrolofthisvectordependsonﬁnancialinvestmentforthe

controlofdengue–whichexceedsR$1bi(US$308m)annually

inBrazilalone(Brazil,2015).Beyonditsroleinthedissemination ofdengueinthiscountry,thisvectorhasrecentlybeeninvolved inthespreadoftheZikaviruswhich,despiteitsrelativelymild symptomatology,can,exceptionally,causeseriousalterationsin thenervoussystemoffetusesintheprocessofgrowth(Brazil,2016; CDC,2016;Mlakaretal.,2016;Rasmussenetal.,2016).Thus,inthe lightofthevariousimpactswhichthisvectorhasbeenmakingon humanhealth,theaccompanimentofitsinfestationinnewareas, ashasbeenhappeninginCruzeirodoSul,providesrelevant infor-mationforthestrategicandspeciﬁcvectorcontrolactionswhich areneededtoprotecttheexistinghumanpopulations.

Thespecieswhichpresentedthelowerfrequenciesinthe

col-lectionsmadeweredistributedrandomlythroughoutthesurveys

undertaken,notallofthemoccurringinparticularsituationsor areas.TheleastfrequentspecieswasTx.theobaldiwhich,inthe

majorityofobservations,wasfoundtobepresenttogetherwith

Ae.albopictus,aresulttobeexpectedseeingthatthespeciesis rec-ognizedasanaggressivepredatoroftheimmatureformsofother mosquitospecies,itscohabitationhavingalreadybeenrecordedin otherstudies(Lopesetal.,1993;Lopes,1997).

Ae.ﬂuviatilisandCx.quinquefasciatusarespecieswhichoccurred inlowfrequencyinthepresentstudy,byvirtueofthe

method-ology employed,but whose anthropophilic habits have already

beendescribedandwhichfrequenttheenvironmentofthe

resi-dences,makinguseofthetrapsplacedtherefortheiregg-laying (ConsoliandLourenço-de-Oliveira,1994;Forattini,2002).Ae. fluvi-atilispossessestheabilitytoinfectwiththeYellowFevervirusinthe laboratoryandCx.quinquefasciatus,aswellasbeingtheprincipal vectorofWuchereriabancroftiontheAmericancontinent,hasalso beenincriminatedinthetransmissionofarboviruses(Consoliand Lourenço-de-Oliveira,1994;Forattini,2002),whichdemonstrates theimportanceofthemonitoringofthesespecies.

Representatives of the Culex Complex Coronator group

accounted for 0.40%of the total larvae collected. Thisgroup is

widely distributed throughout theAmericas and uses breeding

places,bothnaturalandartiﬁcial,whetherwithcleanorpolluted

speciesoccursinurbanenvironments(Silvérioetal.,2007)and isrelatedtothetransmissionofSt.Louisencephalitis(Fernandez etal.,2000).

Itwasonlypossibletoundertaketheanalysisofdiversityin theareasofCruzeirodoSul,ValedasCigarrasandSantaAliceby virtue ofthenumber oftraps existingthere fortheapplication ofthismethod.Intheseplaces,bymeansofthemapsgenerated, itwasfoundthatintheregionswithineachoftheareaswhere Ae.aegyptipresentedgreaterabundancethediversityvalueswere lower.Theproximityofmorehighlyvegetatedareasincreasedthe Simpson’sdiversityvaluesobtained,whereasAe.aegyptipresents greateroccurrenceinparticularregionswithintheareasstudied here,closertourbannucleiandtheiraccessroads.Theresidents’ vehicletrafﬁcmayofferconditionsfavorabletothisgreater abun-danceofthespeciesasitofferspassivetransportforthespecies whichalsoproﬁtsfromtheecologicaladvantageswhichthe envi-ronment(Julianoetal.,2002)–oreventhehumanbeinghimself– provides(Lounibosetal.,2010)toexpanditsdistributioninthese areas.

InCruzeirodoSul,thegreaterdiversityvaluesobservedwere foundinthewestofthearea,whichcorroboratestheresultssetout inanearlierstudyofthelocality(Piovezanetal.,2013).The

accom-panimentofthemosquitopopulationsisafundamentalnecessity

fortheestablishmentofstrategicmeasureswhichwillminimize

therisksrunbythehumanpopulation.Differentialcontroland pre-ventionactivitiesshouldcertainlybecarriedoutinthoselocalities whichretaintheirrelationshipwiththenaturalenvironmentbut whichalso,atthesametime,possesssomeurbanstructure.These locationsnotareneitherexclusivelyurbanorrural,andthevector controlintheseareasshouldbedifferentiatedfromthatwhichis oftenpresentedinthemanuals.

Itshouldbenotedthattheworkofvectorcontroltobe under-takenintheruralareascallsforadaptation,seeingthatthereexist criticaldifferencesintermsofscenery,ofavailablebreedingplaces, oftheecologicalrelationshipsestablishedintheseenvironments andoftheenvironmentalandanthropicconditionspropertothese areas.Certainlyintheseareas,entomologicalandepidemiological surveillanceactivitiesarethebasictoolsfortheminimizationof epidemicrisks.Themonitoringofinformationonthediseasesand

vectorswhichmaybefoundintheseareascanhelponbothwork

fronts:theﬁrstpermittingthatlocalauthoritiesworkwith pub-licityandpedagogicalconcepts,expandingtheknowledgeofwhat needstobedonebythelocalresidentpopulationitselftoreduce riskand,secondly,providingelementsforcontrolactionsinthe areasofgreaterpriorityorrisk.

WithintheﬁeldofthediscussionofthecontrolofAe.aegypti,in thefaceofthenewrisksofthetransmissionofarbovirusestoday bothinBrazilandintheWorldasawhole,itisimperativethat themethodsappliedinthisﬁghtshouldberevisedandreassessed

andrevised.Thelongbattlewagedonthismosquitovectorhas

achievedsomesuccesses,butasaruleithasbeenlostandthis hashadanegativeimpactonsociety.Thisarticlepresentssome considerationsastowhatcanbedoneintransitionalenvironments, whicharenewfrontiersofoccupationforAe.aegypti,butwhich alsopresentthepresenceofspeciessuchasAe.albopictus,which hasincreasedtheprobabilityofitsinfectionanddisseminationof arbovirusesunderconditionsofcompetition(Juliano,2009).

Inurbanenvironments,controlmethodsaregreatlyinﬂuenced bythebehaviorofthehumanpopulation.Itiscommonlyfoundthat 35%ormoreofresidencesarenotvisitedduringmosquitocontrol operationsbyreasonoftheabsenceoftheresidentontheoccasion ofthevisit.Theefﬁciencyofcontroloperationscallsforthe

adop-tionofmeanswhichwillminimizetheseproblemsandwhichwill

informthepopulationthatiftheyarecarriedouttheywillhelp

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thatourstudiesshouldnowbedirectedtothequantiﬁcationand qualiﬁcationoftheeffortandinvestmentmadebypublic author-itieswithaviewtothecontrolofAe.aegypti.Thisnewresearch

shouldpresentoperationalandﬁnancialinformationwhichwill

contributeinsuchawayastoenablethemanagertochoosethe methodmostappropriatetohisﬁnancialcondition,aswellas satis-fyingthosetechnicalconceptswhoseefﬁcacyincontrolhavebeen proven.

Conﬂictsofinterest

Theauthorsdeclarenoconﬂictsofinterest.

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