Monthly Distribution of Phlebotomine Sand Flies, and Biotic and Abiotic Factors Related to Their

17 Pages·2016·2.15 MB·English

RESEARCHARTICLE
Monthly Distribution of Phlebotomine Sand
Flies, and Biotic and Abiotic Factors Related
to Their Abundance, in an Urban Area to
Which Visceral Leishmaniasis Is Endemic in
Corumba´, Brazil
EvertonFalcãodeOliveira1,4☯*,AlineEtelvinaCasaril2‡,WagnerSouzaFernandes2‡,
MichelledeSaboyaRavanelli3‡,Ma´rcioJose´deMedeiros4☯,RobertoMacedoGamarra5☯,
a11111
AntoˆnioConceic¸ãoParanhosFilho5‡,ElisaTeruyaOshiro2‡,AlessandraGutierrez
deOliveira2‡,EuniceAparecidaBianchiGalati1,6☯*
1 ProgramadePo´s-Graduac¸ãoemSau´dePu´blica,FaculdadedeSau´dePu´blica,UniversidadedeSão
Paulo,SãoPaulo,SP,Brasil,2 Laborato´riodeParasitologiaHumana,CentrodeCiênciasBiolo´gicaseda
Sau´de,UniversidadeFederaldeMatoGrossodoSul,CampoGrande,MS,Brasil,3 AgênciaEstadualde
DefesaSanita´riaAnimaleVegetal,IAGRO,Corumba´,MS,Brasil,4 DepartamentodeEstat´ıstica,Campus
Macae´,UniversidadeFederaldoRiodeJaneiro,Macae´,RJ,Brasil,5 Laborato´riodeGeoprocessamento
OPENACCESS paraAplicac¸õesAmbientais,FaculdadedeEngenharias,ArquiteturaeUrbanismoeGeografia,
UniversidadeFederaldeMatoGrossodoSul,CampoGrande,MS,Brasil,6 Departamentode
Citation:FalcãodeOliveiraE,CasarilAE, Epidemiologia,FaculdadedeSau´dePu´blica,UniversidadedeSãoPaulo,SãoPaulo,SP,Brasil
FernandesWS,RavanelliMdS,MedeirosMJd,
GamarraRM,etal.(2016)MonthlyDistributionof ☯Theseauthorscontributedequallytothiswork.
PhlebotomineSandFlies,andBioticandAbiotic ‡Theseauthorsalsocontributedequallytothiswork.
FactorsRelatedtoTheirAbundance,inanUrban *[email protected](EFO);[email protected](EABG)
AreatoWhichVisceralLeishmaniasisIsEndemic
inCorumba´,Brazil.PLoSONE11(10):e0165155.
doi:10.1371/journal.pone.0165155 Abstract
Editor:MarceloGustavoLorenzo,Fundacao
OswaldoCruz,BRAZIL Themonthlydistributionandabundanceofsandfliesareinfluencedbybothbioticandabi-
Received:July7,2016 oticfactors.Thepresentstudyaimedtoevaluatetheseasonaldistributionofsandfliesand
therelationbetweentheirabundanceandenvironmentalparameters,includingvegetation
Accepted:October8,2016
andclimate.Thisstudywasconductedovera2-yearperiod(April2012toMarch2014).
Published:October26,2016
MonthlydistributionwasevaluatedthroughtheweeklydeploymentofCDClighttrapsinthe
Copyright:©2016FalcãodeOliveiraetal.Thisis peridomicileareaof5residencesinanurbanareaofthemunicipalityofCorumba´ inthe
anopenaccessarticledistributedundertheterms
StateofMatoGrossodoSul,Brazil.MeteorologicaldatawereobtainedfromtheMato
oftheCreativeCommonsAttributionLicense,
whichpermitsunrestricteduse,distribution,and GrossodoSulCenterforWeather,Climate,andWaterResources.Thespectralindices
reproductioninanymedium,providedtheoriginal werecalculatedbasedonspatialresolutionimages(GeoEye)andthepercentageofvege-
authorandsourcearecredited.
talcoverage.Differencesintheabundanceofsandfliesamongthecollectionsiteswere
DataAvailabilityStatement:Allrelevantdataare assessedusingtheKruskal-Wallistest,andthestrengthofcorrelationsbetweenenviron-
withinthepaper.
mentalvariableswasdeterminedbycalculatingSpearman’scorrelationcoefficients.Lutzo-
Funding:Thisworkwassupportedbygrantsfrom myiacruzi,Lu.forattinii,andEvandromyiacorumbaensiswerethemostfrequentlyfound
theSãoPauloResearchFoundation(FAPESP
species.Althoughnosignificantassociationwasfoundamongthesesandflyspeciesand
2011/23414-0),theFoundationforDevelopment
thetestedenvironmentalvariables(vegetationandclimate),highpopulationpeakswere
SupportofEducation,ScienceandTechnologyof
theStateofMatoGrossodoSul(FUNDECT/DECIT- foundduringtherainyseason,whereaslowpeakswereobservedinthedryseason.The
MS/CNPq/SESN˚04/2013–PPSUS-MS–23/ monthlydistributionofsandflieswasprimarilydeterminedbyLu.cruzi,whichaccounted
200.537/2013),andtheBrazilianNationalCouncil
PLOSONE|DOI:10.1371/journal.pone.0165155 October26,2016 1/17
BioticandAbioticFactorsRelatedtotheAbundanceofSandFlies
forScientificandTechnologicalDevelopment for93.94%ofthespecimenscollectedeachmonththroughouttheexperimentalperiod.
(CNPq304122/2015-7). Thefactthatsandfliesweredetectedyear-roundindicatesacontinuousriskofinfectionto
CompetingInterests:Theauthorshavedeclared humans,demonstratingtheneedfortargetedmanagementandeducationprograms.
thatnocompetinginterestsexist.
Introduction
Themonthlydistributionandabundanceofsandfliesisinfluencedbybothbioticandabiotic
factors.Temperature, humidity,andrainfallexertadirectinfluenceonsandflypopulations,
witheffectsbeingdependentontheregion,weather,andspeciesanalyzed[1–4].
Geospatialtools,geographicinformationsystems(GIS),andgeostatisticshavefacilitated
studiesonhowhealth,theenvironment,andsocioeconomicconditionsarerelatedwiththe
temporalandspatialdistributionsofdifferentdiseasesandvectorpopulations[2,5–8].Such
studieshaveprovidedimportantinformationforhealthsurveillance,providingdataformoni-
toringandmappingriskfactors,aswellasprovidingbetterdescriptions,understanding,and
predictionsofgeographicdistribution[5,7,8].
Differentspectralindices,whicharecalculatedfromtherelationshipofdifferentbandsof
satelliteimages,allowustoobtainspecificinformationaboutlandcover,suchasthepresence
ofurbanizedareasorbodiesofwater,vegetalcoverage,andleafarea[9,10].Useofdata
obtainedfromsatelliteimages,suchasthenormalizeddifferencevegetationindex(NDVI),has
allowedtheidentificationandmonitoringofvegetationdiversity,aswellasthedetermination
ofgeographicalspaceandareasatriskofendemicdiseases,suchasvisceralandcutaneous
leishmaniasis,andhowtheyaffectvectorpopulations[2,6,7,11,12].
InSouthAmerica,thespatialdistributionpatternofLutzomyialongipalpisispositively
associatedwiththepresenceofvegetationintheperidomesticenvironment[3,13].InEurope,
Asia,andAfrica,weatherdataandremotesensinghavebeenusedtopredictthegeographic
andseasonaldistributionofPhlebotomusspp.,withthesespatialvariablesbeingstronglycorre-
latedwithspeciespresence[11,12,14].
Thisstudyaimedtoevaluatetheseasonaldistributionofsandflies,aswellastoinvestigate
possibleassociationsbetweenthemostabundantspeciesandenvironmentalvariablesrelated
tovegetationandclimate.
MaterialsandMethods
StudyArea
ThisstudywasconductedintheurbanareaofthemunicipalityofCorumbá,whichislocated
inthenortheasternpartoftheStateofMatoGrossodoSul,Brazil,intheregionofthePantanal
wetland,ontheborderofBoliviaandadjacenttotheParaguayRiver(19°00033@ʹS;57°39012@
O;118mabovesealevel;Fig1).Theurbanregionofthemunicipalitywasconsideredtobe
thatcharacterizedbycontinuousbuildingsandtheexistenceofsocialinfrastructuresforbasic
urbanfunctions(e.g.,housing,work,recreation,andcirculation).AccordingtotheBrazilian
InstituteofGeographyandStatistics,themunicipalitywasestimatedtobeinhabitedbyapop-
ulationof108,010in2014,withademographicdensityof1.60inhabitants/km2,90%ofwhich
residedintheurbanarea[15].
TheurbanareaofthemunicipalityislocatedinamountainousregionknownasMorraria
doUrucum,inanareaofsubmontanedeciduousforest.Thepredominantvegetalcoverageis
theBrazilianCerrado,whichisasavannah-likebiometypicalofthePantanalwetland[16].
PLOSONE|DOI:10.1371/journal.pone.0165155 October26,2016 2/17
BioticandAbioticFactorsRelatedtotheAbundanceofSandFlies
Fig1.SpatialdistributionofsandflysamplingsitesintheurbanareaofCorumba´,MatoGrossodo
Sul,Brazil.Numbers1–5indicatesandflysamplingsites(neighborhoods):1=Center;2=MariaLeite;
3=CristoRedentor;4=PopularNova;5=NovaCorumba´.TheurbanareaofthemunicipalityofCorumba´is
representedbyaGeoEyeimageinfalse-colorcompositionRGB432(20/08/2012).Note:themapofBrazil
(andtheshapefileusedtogenerateit)usedfortheelaborationofFig1wasextractedfromthedatabaseof
publicdomainoftheBrazilianInstituteofGeographyandStatistics(http://mapas.ibge.gov.br/bases-e-
referenciais.html).
doi:10.1371/journal.pone.0165155.g001
AccordingtotheKöppenclassificationsystem,theclimateofthemunicipalityofCorumbá
istropical(Aw)andmegathermal,withadrywinterandwetsummer[17].Thedryseason
runsfromApriltoSeptember,andtherainyseasonrunsfromOctobertoMarch[18].
SandFlyCollection
SandflieswerecollectedweeklyfromApril2012toMarch2014usingCDCautomaticlight
traps.Thesamplingsitesconsistedoftheperidomiciliaryareasof5residenceslocatedinneigh-
borhoodswhereatleast1humancaseofvisceralleishmaniasiswasreportedin2011(Fig1).
Table 1summarizesthecharacteristicsofeachsamplingsite.Twotrapsweredeployedineach
samplingsitebetween17:00and07:00thenextmorning.Samplingtimepertrapwas1,050h,
andthetotalsamplingtimewas105,000h.
ThespecimenswereidentifiedaccordingtotheclassificationsystemofGalati[19].Generic
nameswereabbreviatedaccordingtoMarcondes[20].Allmalescollectedduringthe2two
years,aswellasfemalescollectedduringthefirst6monthsof2012,wereslide-mountedfor
identification.Thereafter,collectedfemalesthatdidnothavebloodintheirgutweredissected,
andidentifiedonthebasisoftheirspermathecacharacteristics.Thesefemaleswerethenplaced
in1.5-mLmicrotubeswithisopropylalcoholtodeterminethepresenceofLeishmaniaDNA,
theresultsofwhicharedescribedbyOliveiraetal.[21].
VegetalCoverageandImperviousSurfaceAreas
FromAugust20,2012,GeoEye-1satelliteimageswith0.4-mresolutionwereusedasthecarto-
graphicbasistodeterminetheenvironmentalvariablesofvegetationandimpervioussurface
areas(ISAs),bothofwhicharefoundwithintheurbanenvironment.Theimageswereortho-
rectifiedandgeometricallycorrectedusingadefinedprojectionanddatum.Theprojection
usedwastheUniversalTransverseMercator, southernhemisphere,Zone21andthedatum
wasWGS84.
Thesebandswerecombinedtogenerateamultispectralimagefromwhichatmosphericcor-
rectioncouldbeperformedtocalculateNDVI,normalizeddifferencewaterindex(NDWI),
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BioticandAbioticFactorsRelatedtotheAbundanceofSandFlies
Table1. Generalcharacteristicsofsamplingsites.
Residence Generalcharacteristics Domesticatedanimals
(neighborhood) (number)
Centro(1)
•Locatedincommercialcenterofthecity; • Dogs(2)
•Largeperidomicileareawithlargetomedium-sizedtrees,someofwhicharefruittrees; • Chicken(1)
•SamplingsiteclosesttoParaguayRiver(approximately500m).
MariaLeite(2)
•Locatedinnortheasternoutskirtsofthecity; • Dogs(2)
•Largerperidomicileareaincomparisontoothersites;largeandmedium-sizedtrees,someof • Chickens(15a)
whicharefruittrees. • Geese(5)
• Ducks(3)
CristoRedentor(3)
•Locatedinsoutheasternperipheryofthecity; • Dog(1)
•Peridomicilearealimitedbytheridgeofthehillscoveredwithnativevegetation,withsome
smalltrees.
PopularNova(4)
•Locatedinsoutheasternperipheryofthecity; • Dog(1)
•Smallerperidomicileareaincomparisontotheothersites;
•Twomedium-sizedfruittrees.
NovaCorumba´(5)
•Locatedinsouthernperipheryofthecity; • Dogs(5)
•Peridomicilearealimitedbyaridgeofhillscoveredwithnativevegetation,withsmalland • Chickens(4)
medium-sizedtrees,someofwhicharefruittrees. • Cats(3)
aThenumberofchickensatthisresidencevariedthroughoutthestudybutwasalwaysgreaterthan15.
doi:10.1371/journal.pone.0165155.t001
andISAaroundthesandflycollectionpoints,withbuffersof100and200m.Theseprocedures
wereperformedusingthesoftwarePCIGeomatica9.1[22].
NDVIvaluesrangedfrom-1to+1,andwerecalculatedusingthefollowingequationpro-
posedbyRouseetal.[23]:
ðNIR(cid:0) RÞ
NDVI ¼
ðNIRþRÞ
inwhichNIRisthereflectanceofvegetationinthenearinfraredbandandRisthereflectance
ofvegetationintheredband.
TheNDVIofeachsamplingsitewasstratifiedtoobtainvariablesrelatedtolandscapeattri-
butesatdifferentscales,suchashabitatcomplexity(meanNDVI)andheterogeneity(standard
deviationofNDVI)[3].Habitatcomplexityisdefinedasthedensityanddevelopmentofthe
verticalstratuminaparticularunitofarea,whilehabitatheterogeneityisthestructureofthe
vegetationonthehorizontalplane[24].
NDWIvaluesalsorangedfrom-1to+1,andwerecalculatedfromthefollowingequation
proposedbyMcFeeters[25]:
ðGREEN(cid:0) NIRÞ
NDWI ¼
ðGREENþNIRÞ
inwhichNIRisthereflectanceofvegetationinthenearinfraredbandandGREENisthereflec-
tanceofvegetationinthegreenband.
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BioticandAbioticFactorsRelatedtotheAbundanceofSandFlies
ISAisthedegreeofimpermeabilityofthesoil,whichwascalculatedfromtheequationby
CarlsonandArthur[26]:
" #
(cid:18) (cid:19)
ðNDVI(cid:0) NDVI Þ 2
ISA¼ 1(cid:0) 0
ðNDVI þNDVI Þ
S 0
dev
inwhichNDVI istheNDVIforexposedsoilandNDVI istheNDVIfordensevegetation.
0 S
Thetermdevindicatesthattheformulaisonlyappropriateforregionsclassifiedasurban,with
numberscloserto1indicativeofgreaterimpermeability.
Percenttreecanopycover(vegetalcoverage)ineachsamplingsitewasestimatedusinga
pointinterceptsphericaldensiometer.Thisequipmentconsistsofasquareconvexmirrorwith
36verticesthatreflectthewoodyvegetationcoveragein4directions(north,south,east,and
west),witheachobservationoccurringat90°rotationinrelationtothepreviouspoint[27].
Thearithmeticmeanofthedatacollectedforall4directionswascalculatedtodeterminethe
percentageofvegetalcoverageusingasimpleruleof3.Ateachcollectionpoint,5random
measurementsweremade.
MeteorologicalData
TheclimatedataforthestudyperiodwereextractedfromtheMatoGrossodoSulCenterfor
Weather, Climate,andWater Resources(www.cemtec.ms.gov.br),whichislinkedtotheBra-
zilianNationalMeteorologicalInstitute.Dailyreadingsoftemperature,relativeairhumidity,
rainfall,andwindvelocitywereobtained.Fortemperatureandhumidity,meandailyreadings
wereconsidered7,15,and30dayspriortothecollectiondate.Similarmethodswereusedto
determinerainfall;however,accumulated(sum)values,ratherthanmeanvalues,wereused.
StatisticalAnalysis
Descriptivemeasuressuchasthegeometricmean(Williamsmeans,Mw)[28,29],arithmetic
mean,median,standarddeviation,minimum,andmaximumwerecalculatedtodescribethe
totalnumberofspecimenscollectedandthe3mostabundantspecies.Thehypothesisofequal-
ityofproportionaldistributionofthetotalnumberofspecimensandthetotalofthe3most
abundantspeciesateachcollectionsiteforbothsexeswereassessedusingtheKruskal-Wallis
test.
TheWilcoxontestwasusedforcomparisonsoftheabsolutefrequenciesofthetotalnumber
ofsandfliesandofthe3mostabundantspeciesstratifiedbysexandseason(dryorrainy).
Theassociationbetweenmeteorologicalvariablesandtheabsolutefrequencyofsandflies
wasevaluatedusingtheSpearmancorrelationcoefficient.Thesameanalysiswasusedtomea-
surethedegreeoflinearrelationshipbetweenthenumberofspeciesobservedandtheenviron-
mentalvariables(vegetationandISA)understudy.
TheanalysiswasconductedusingRsoftwareversion3.3.0[30]andbyemployinga5%
(α=0.05)significancelevel.
EthicalStatement
ThisstudyreceivedtheapprovaloftheAnimalExperimentationEthicsCommitteeoftheFed-
eralUniversityofMatoGrossodoSul(Brazil),underprocessnumber491/2013.Theresearch
grouphasapermanentlicenseforthecollectionofzoologicalmaterial,issuedbytheBrazilian
InstituteoftheEnvironmentandRenewableNaturalResources(IBAMA:SISBio25952–1).
Fieldstudieswerecarriedouton5privateproperties,theownersofwhichgavepermissionto
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BioticandAbioticFactorsRelatedtotheAbundanceofSandFlies
conductthestudyintheirrespectiveperidomiciliaryareas.Inaddition,thefieldstudiesdidnot
involveanyendangeredorprotectedspecies.
Results
Atotalof750weeklycollectionswereperformedfromApril2012toMarch2014,through
which14,317specimensofsandflieswerecaught:7,370specimensduring390collectionsin
thefirstyearand6,947specimensduring360collectionsinthesecondyear.Thespecimens
weredistributedamong8genera(Brumptomyia,Evandromyia,Lutzomyia,Micropygomyia,
Martinsmyia,Nyssomyia,Psathyromyia,andSciopemyia)andrepresented13species(Table 2).
ThisstudyprovidesthefirstreportofNy.whitmaniinthestudyregion.
Table 3presentsthedescriptivemeasuresforthetotalnumberofsandfliescaughtandthe3
mostabundantspeciesateachcollectionsite.Inallcases(totalandspeciesanalysis),theKrus-
kal-Wallistestrevealedthatthemonthlyarithmeticmeandifferedbetweenthecollectionsites,
withoneormoresitesstandingoutintermsofsandflyabundance.Geometricmeans(Wil-
liamsmeans,Mw)demonstratedthesameresult.Owingtothesedifferences,thetotalnumber
ofsandflieswasanalyzedinaconditionalmanner.
Lu.cruziwasthemostfrequentlycollectedspecies,accountingfor93.94%ofthetotal,fol-
lowedbyLu.forattinii (3.22%)andEv.corumbaensis(1.76%).Thisrankingofabundancewas
foundatallcollectionsites.Proportionally,malesweresignificantlymoreabundantthan
females(W=65,797;p<0.001).Thisproportionheldtruewhenanalyzingthe3mostfrequent
speciesseparately:Lu.cruzi(W=66,444.50;p<0.001),Lu.forattinii (W=48,327.0;p=0.006),
andEv.corumbaensis(W=38,346.50;p<0.001).
ThegeometricmeansofmonthlydistributionofLu.cruzi,Lu.forattinii, andEv.corum-
baensisandthemonthlyarithmeticmeansoftheclimatevariables(exceptrainfall,whichwas
consideredintermsofmonthlyaccumulation)arepresentedinFig2.Throughoutthestudy
period,theannualaveragetemperaturewas26.24°C,theannualaveragerelativeairhumidity
Table2. Absolutefrequencyofsandfliesaccordingtosex,samplingsite(neighborhood),andspeciesrichnessofthesamplingsite.
Species Samplingsite Total
Centro MariaLeite CristoRedentor PopularNova NovaCorumba´
♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀
Br.brumpti - - - - - - - - 2 2 4
Ev.aldafalcaoae 2 3 - 1 1 - - - - 1 8
Ev.cortelezzii - 1 - 1 - 1 - 2 - 2 7
Ev.corumbaensis 9 48 8 22 21 63 10 27 8 36 252
Ev.sallesi 1 5 3 7 3 3 - 2 - 2 26
Ev.walkeri 1 1 - 1 - - - - - 2 5
Lu.cruzi 3,100 548 4,004 417 1,151 233 389 100 2,996 511 13,449
Lu.forattinii 14 9 17 12 158 61 3 10 63 114 461
Mi.peresi 1 2 1 2 23 9 7 4 11 8 68
Mt.oliveirai - - - 1 12 3 3 3 1 4 27
Ny.whitmani - - - - - - - - - 1 1
Pa.bigeniculata - - - - 2 1 - - - 1 4
Sc.sordellii - - - 1 - 1 - 1 - 2 5
Total 3,128 617 4,033 465 1,371 375 412 149 3,081 686 14,317
Speciesrichness 8 10 10 8 13 -
Br:Brumptomyia;Ev.:Evandromyia;Lu:Lutzomyia;Mi:Micropygomyia;Mt:Martinsmyia;Ny.:Nyssomyia;Pa.:Psathyromyia;Sc.:Sciopemyia.
doi:10.1371/journal.pone.0165155.t002
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Table3. Descriptivemeasuresoftotalnumberofsandflies,aswellaspopulationsofEv.corumbaensis,Lu.cruzi,andLu.forattinii,withrespect
tosamplingsite(neighborhood).
Species Samplingsite Arithmeticmean Williamsmean Standarddeviation Median Minimum Maximum p-valuea
Ev.corumbaensis(F)
Centro 0.64 0.33 1.28 0 0 8 0.142
CristoRedentor 0.84 0.37 1.87 0 0 10
MariaLeite 0.29 0.17 0.67 0 0 3
NovaCorumba´ 0.48 0.25 1.00 0 0 4
PopularNova 0.36 0.20 0.86 0 0 6
Total 0.52 0.27 1.22 0 0 10
Ev.corumbaensis(M)
Centro 0.12 0.07 0.43 0 0 2 0.035
CristoRedentor 0.28 0.17 0.58 0 0 2
MariaLeite 0.11 0.07 0.39 0 0 2
NovaCorumba´ 0.11 0.07 0.39 0 0 2
PopularNova 0.13 0.08 0.53 0 0 4
Total 0.15 0.09 0.47 0 0 4
Ev.corumbaensis(MF)
Centro 0.76 0.36 1.50 0 0 9 0.083
CristoRedentor 1.12 0.48 2.20 0 0 12
MariaLeite 0.40 0.24 0.74 0 0 3
NovaCorumba´ 0.59 0.30 1.13 0 0 5
PopularNova 0.49 0.26 1.11 0 0 6
Total 0.67 0.33 1.44 0 0 12
Lu.cruzi(F)
Centro 7.31 1.41 10.13 3 0 38 <0.001
CristoRedentor 3.11 0.91 5.74 1 0 40
MariaLeite 5.56 1.17 12.03 2 0 93
NovaCorumba´ 6.81 1.32 12.13 3 0 65
PopularNova 1.33 0.59 1.88 0 0 8
Total 4.82 1.08 9.51 1 0 93
Lu.cruzi(M)
Centro 41.33 2.45 96.50 15 0 750 <0.001
CristoRedentor 15.35 1.55 34.94 2 0 192
MariaLeite 53.39 2.58 112.04 17 0 689
NovaCorumba´ 39.95 2.36 64.65 8 0 310
PopularNova 5.19 1.20 8.08 2 0 48
Total 0.00 0.00 0.00 0 0 0
Lu.cruzi(MF)
Centro 48.64 2.69 103.60 22 0 787 <0.001
CristoRedentor 18.45 1.81 39.95 4 0 232
MariaLeite 58.95 2.73 117.22 18 0 696
NovaCorumba´ 46.76 2.58 73.79 11 0 361
PopularNova 6.52 1.37 9.18 4 0 53
Total 35.86 2.24 81.54 7 0 787
Lu.forattinii(F)
Centro 0.12 0.06 0.57 0 0 4 <0.001
CristoRedentor 0.81 0.36 1.85 0 0 12
MariaLeite 0.16 0.10 0.49 0 0 3
NovaCorumba´ 1.52 0.34 6.63 0 0 54
PopularNova 0.13 0.08 0.47 0 0 3
Total 0.55 0.19 3.14 0 0 54
(Continued)
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BioticandAbioticFactorsRelatedtotheAbundanceofSandFlies
Table3. (Continued)
Species Samplingsite Arithmeticmean Williamsmean Standarddeviation Median Minimum Maximum p-valuea
Lu.forattinii(M)
Centro 0.19 0.08 1.00 0 0 8 <0.001
CristoRedentor 2.11 0.62 4.45 0 0 24
MariaLeite 0.23 0.14 0.56 0 0 3
NovaCorumba´ 0.84 0.37 1.82 0 0 10
PopularNova 0.04 0.02 0.26 0 0 2
Total 0.68 0.24 2.33 0 0 24
Lu.forattinii(MF)
Centro 0.31 0.12 1.46 0 0 12 <0.001
CristoRedentor 2.92 0.83 5.32 1 0 25
MariaLeite 0.39 0.22 0.84 0 0 4
NovaCorumba´ 2.36 0.56 7.91 0 0 64
PopularNova 0.17 0.10 0.53 0 0 3
Total 1.23 0.37 4.47 0 0 64
Total(F)
Centro 8.23 1.57 10.65 4 0 39 <0.001
CristoRedentor 5.00 1.20 8.59 2 0 60
MariaLeite 6.20 1.27 12.69 2 0 98
NovaCorumba´ 9.13 1.50 17.42 4 0 107
PopularNova 1.99 0.76 2.58 1 0 12
Total 6.11 1.26 11.69 2 0 107
Total(M)
Centro 41.71 2.48 96.52 16 0 750 <0.001
CristoRedentor 18.28 1.82 38.02 4 0 204
MariaLeite 53.77 2.60 112.64 17 0 696
NovaCorumba´ 41.08 2.45 65.96 9 0 320
PopularNova 5.49 1.25 8.40 3 0 51
Total 32.07 2.12 76.31 6 0 750
Total(MF)
Centro 49.93 2.80 103.90 24 0 789 <0.001
CristoRedentor 23.28 2.14 44.91 7 0 264
MariaLeite 59.97 2.77 118.16 19 0 704
NovaCorumba´ 50.21 2.72 79.58 18 0 427
PopularNova 7.48 1.50 9.79 5 0 57
Total 38.18 2.38 83.40 10 0 789
aKruskal-Wallistest;F=females;M=males;MF=sumofmalesandfemales;Ev:Evandromyia;Lu:Lutzomyia.
doi:10.1371/journal.pone.0165155.t003
was67.43%,andtheaccumulatedrainfallwas2,312.80mm3.Table 4presentstheclimaticvari-
abledata.Nosignificantassociationwasfoundbetweentheabsolutefrequencies(totalandper
species)ofsandfliesandmeteorologicalvariables,evenafterconsideringallassessedderiva-
tions(dailymeanofthecollectiondateandmeansmeasuredat7,15,and30dayspriortoeach
collectiondate).Intheanalysisofabundanceaccordingtoseason,onlyEv.corumbaensis
femalesfailedtoconfirmthehypothesisofequalitybetweenseasons(W=503,50;p=0.05).
However,4highpopulationpeakswerefoundintherainyseasonand2smallerpopulation
peakswerefoundinthedryseasonforLu.cruzi.Likewise,2populationpeakswerefoundin
therainyseasonforbothLu.forattinii andEv.corumbaensis.
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BioticandAbioticFactorsRelatedtotheAbundanceofSandFlies
Fig2.MonthlydistributionofLu.cruzi,Lu.forattinii,andEvcorumbaensisandthemonthly
arithmeticmeanoftheclimatevariablesainCorumba´,MatoGrossodosul,Brazil,betweenApril
2012toMarch2014.aRainfallwasconsideredintermsofmonthlyaccumulation.
doi:10.1371/journal.pone.0165155.g002
Table 5presentsthevegetationandISAindicesobtainedthoughremotesensing,andthe
percentageofvegetalcoveragecalculatedusingasphericaldensiometer.Nosignificantassocia-
tionwasfoundbetweentheabsolutefrequenciesofsandfliesandanyofthestudiedvariables,
includinghabitatcomplexityandhabitatheterogeneity.
Discussion
Althoughthefirstcaseofhumanvisceralleishmaniasiswasrecordedin1911[1,31]inthe
PortoEsperançadistrictofthemunicipalityofCorumbá,studiesonsandflyfaunainthiscity
onlybeganinthe1980s[32,33].Duringthisperiod,12specieswereidentified,withLu.cruzi
andLu.forattinii beingthemostabundantinurbanareas[8,32–34].Lu.longipalpiswas
PLOSONE|DOI:10.1371/journal.pone.0165155 October26,2016 9/17
BioticandAbioticFactorsRelatedtotheAbundanceofSandFlies
Table4. DescriptivemeasuresofmeteorologicalvariablesinCorumba´,MatoGrossodoSul,betweenApril2012toMarch2014.
Variable Arithmeticmean Standarddeviation Median Minimum Maximum
Temperature
Collectionday 26.10 3.97 27.04 13.77 34.08
Previous7 25.71 2.99 26.50 17.75 32.56
Previous15 25.61 2.57 26.10 19.59 31.14
Previous30 25.65 2.30 25.96 21.40 29.60
Humidity
Collectionday 65.76 14.08 69.46 33.38 89.00
Previous7 66.61 12.21 68.55 37.55 85.54
Previous15 66.71 11.56 69.48 36.92 85.33
Previous30 66.68 9.94 69.53 42.47 81.81
Rainfall
Collectionday 0.55 2.65 0.00 0.00 21.00
Previous7 16.27 27.46 2.80 0.00 168.00
Previous15 26.74 35.96 11.80 0.00 170.40
Previous30 73.11 68.99 49.40 0.00 273.00
Wind
Collectionday 15.16 5.67 14.76 0.00 35.64
doi:10.1371/journal.pone.0165155.t004
Table5. Descriptivemeasuresofenvironmentalvariablesinrelationtosamplingsite,inCorumba´,MatoGrossodoSul,Brazil.
Variable Samplingsite
Centro CristoRedentor MariaLeite NovaCorumba´ PopularNova
VC(%) 79.34 40.83 57.90 77.34 50.83
NDVI(buffer100m)
Mean -0.01 0.01 -0.06 -0.02 -0.09
SD 0.23 0.18 0.18 0.17 0.18
NDVI(buffer200m)
Mean -0.04 -0.01 -0.07 -0.02 -0.07
Standarddeviation 0.23 0.18 0.18 0.15 0.18
NDWI(buffer100m)
Mean -0.12 -0.18 -0.15 -0.18 -0.13
SD 0.20 0.15 0.15 0.15 0.16
NDWI(buffer200m)
Mean -0.11 -0.17 -0.14 -0.19 -0.13
SD 0.20 0.14 0.15 0.13 0.16
ISA(buffer100m)
Mean 0.76 0.83 0.79 0.82 0.73
SD 0.25 0.18 0.21 0.20 0.23
ISA(buffer200m)
Mean 0.73 0.83 0.75 0.83 0.75
SD 0.26 0.18 0.22 0.18 0.23
VC:vegetalcoverage;SD:standarddeviation;NDVI:normalizeddifferencevegetationindex;NDWI:normalizeddifferencewaterindex;ISA:impervious
surfaceareas.
doi:10.1371/journal.pone.0165155.t005
PLOSONE|DOI:10.1371/journal.pone.0165155 October26,2016 10/17