Mapping of spatiotemporal distribution of Tibraca limbativentris Stal (Hem.: Pentatomidae) in flooded rice crop in Southern 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

Biology,

Ecology

and

Diversity

Mapping

of

spatiotemporal

distribution

of

Tibraca

limbativentris

Stal

(Hem.:

Pentatomidae)

in

ﬂooded

rice

crop

in

Southern

Brazil

Helen

da

Silva

Costa

a

_,

_Enio

_Júnior

_Seidel

a

_,

_Juliano

_de

_Bastos

_Pazini

b,∗

_,

_Augusto

_Maciel

_da

_Silva

a

_,

Fernando

Felisberto

da

Silva

b

_,

_José

_Francisco

_da

_Silva

_Martins

c

_,

_José

_Alexandre

_Freitas

_Barrigossi

d

a_Universidade_Federal_de_Santa_Maria_(UFSM),_Centro_de_Ciências_Naturais_e_Exatas_(CCNE),_Departamento_de_{Estatística,}_Cidade_{Universitária,}_Santa_Maria,_Rio_Grande_do_Sul,_RS,

Brazil

b_Universidade_Federal_do_Pampa_(UNIPAMPA),_Campus_Itaqui,_Itaqui,_Rio_Grande_do_Sul,_RS,_Brazil

c_Empresa_Brasileira_de_Pesquisa_{Agropecuária}_(Embrapa),_Embrapa_Clima_Temperado,_Pelotas,_Rio_Grande_do_Sul,_RS,_Brazil d_Empresa_Brasileira_de_Pesquisa_{Agropecuária}_(Embrapa),_Embrapa_Arroz_&_Feijão,_Santo_Antônio_de_Goiás,_Goiás,_GO,_Brazil

a

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i

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l

e

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Articlehistory:

Received11October2018 Accepted18April2019 Availableonline9May2019 AssociateEditor:RegianeBueno Keywords:

Insectecology Multiquadricequations OryzasativaL. Pestmonitoring Ricestembug

a

b

s

t

r

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Thericestembug,TibracalimbativentrisStal(Hem.:Pentatomidae),isoneofthemaininsectpestsin Brazilianricecrops.Knowledgeofitsspatiotemporaldistributioncansupportthedevelopmentofan effectivesamplingsystemandimproveIPMstrategies.Thisstudyaimedtomapthespatiotemporal distributionofricestembuginﬂoodedricecropinSouthernBrazil.Floodedricecropwasscoutedfor twoseasonstoestimateinsectdensities.Fouroccurrencecategorieswereobserved:noinsect,only adults,onlynymphs,andbothphases.Therelationshipbetweenphenologicalstagesandinsectcategories wasestablished.Interpolation(mapping)ofoccurrencecategoriesofT.limbativentriswasperformedby multiquadricequations.Intwoseasonsduringthericecycle,theresultsindicatethatricestembug “adults”werethemostabundantcategoryuntilthemid-vegetativephaseoftherice;“nymphs”were themostabundantfromtheendofvegetativephase;“adults+nymphs”occurredfromthebeginning ofreproductivephase;therewerenoricestembugsinmorethan66%ofthearea,astheyweremost concentratedneartheedgeofthecrop.Theinformationpresentedhereprovidesfurtherknowledge aboutT.limbativentrisspatiotemporaldynamicsthatcanbeappliedtoimproveIPMstrategies,suchas developingsamplingplansandlocalizedcontrolmeasuresattheedgeofriceﬁelds.

Introduction

Rice(OryzasativaL.)isthemostconsumedfoodandthesecond mostcultivatedcerealintheworld,withanareaof168million hectares.Amongthetenlargestproducersintheworld,Brazilisthe onlyriceproducernotlocatedontheAsiancontinent(FAOSTAT, 2016).Rice issocioeconomically importantin Brazilasa staple foodinthepopulation’sdiet.About80%ofitsdomestic produc-tioncomesfromﬂood-irrigatedﬁeldsin1.2millionhectaresinthe Southregion,wherethestateofRioGrandedoSulaccountsfor morethan70%ofBrazilianriceproduction(CONAB,2018).

∗ Correspondingauthor.Presentaddress:UniversidadeFederaldePelotas(UFPel), FaculdadedeAgronomia“EliseuMaciel”(FAEM),DepartamentodeFitossanidade (DFs),CampusUniversitário,AvenidaEliseuMaciel,CaixaPostal354,CEP 96010-900,Pelotas,RioGrandedoSul,RS,Brazil.

E-mail:julianopazzini@hotmail.com(J.B.Pazini).

Tibracalimbativentris Stal (Hem.: Pentatomidae) is a species harmfultoriceﬁeldsindifferentcountriesdistributed through-outtheNeotropicalregion(Martinsetal.,2004).Inaddition,itis amongtheﬁveeconomicallyimportantspeciesofphytophagous stinkbugswithahighpotentialforpropagationincountriesthat havenotyetrecordedtheiroccurrence,suchastheUnitedStates

(Panizzi,2015).InBrazilianriceﬁelds,ricestembugisaninsectpest

ofprimaryoccurrencethatcancausegrainyieldlossesofupto90%

(Ferreiraetal.,1997)duetothefeedingofadultsandnymphson

plantstems(KrinskiandFoerster,2017).“Dead-heart”symptoms arisewhentheypiercethestemsinthevegetativestages,while “white panicle” symptoms occurwhen theypierce the already developedstemsinthereproductivestages(Ferreiraetal.,1997;

Reunião,2016).

Thecontrol of therice stembug is usuallycarried out with pyrethroid andneonicotinoid insecticides(Martinsetal.,2016). Adequatemonitoringofinsectpopulationgrowthinriceﬁeldsis essentialforacorrectdecision tocontrolandreducecrop dam-age.Forthis,determiningthespatiotemporaldistributionofthis https://doi.org/10.1016/j.rbe.2019.04.001

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insectisimportantinformationforIntegratedPestManagement (IPM),aswellastheestablishmentofeffectivesamplingprocesses andpotentialforlocalizedcontrolactions,tominimizeproduction costsandrisksofenvironmentalcontaminationbyinsecticides.

Thespatialdistributionofanorganismisanecological charac-teristiclargelyinﬂuencedbybirth,mortality,andmigrationrates

(Toledoetal.,2006).Spatialdistributionistheformthese

organ-ismsaredispersedintheirnaturalhabitat(Pazinietal.,2017).In apioneeringstudy,CostaandLink(1992)assessedthe spatiotem-poraldistributionofricestembugadultsandemphasizedthatthe vegetativeandreproductivephenologicalstagesofriceplantsmay haveinﬂuencedtheirmodelofdispersionin thecrop. Recently,

Alvesetal.(2016)pointedoutthattheimmatureandadultstages

ofthis insectmay havedifferentdispersions, notalwaysfound onthesame plant or samplingpoint in rice ﬁelds of northern Brazil.Pazinietal.(2017)foundanaggregatespatialdistribution foradults,nymphs,andadultandnymphphasestogether, regard-lessofplantphenologyinricepaddiesofsouthernBrazil.These studiesevidencedquantitativedifferencesintheoccurrenceofT. limbativentrisatdifferenttimesofthericecropcycle(phenological stages),e.g.non-occurrenceoftheinsect,presenceofadultsonly, presenceofnymphsonly,orcoexistenceofbothphases.

TraditionaltechniquesofGeostatisticsbylinearkriging have beenappliedinAgriculturalEntomologytomapthedistribution oforganismsinaspacewhenthetargetvariablesofthestudyare insectdensity(insectcounts)(Pazinietal.,2015a;Alvesetal.,2016;

Piasetal.,2017;Pasinietal.,2018).However,thereareno

stud-iesforcategoricaldata,suchastheoccurrenceofpestinsectsin theimmatureoradultphaseorthecoexistenceofthesephases predominantincropsegmentsthroughoutthecropcycle. Under-standingthe way that the rice stem bug is distributed in rice ﬁeldsinthespaceandtimeprovidedbymappingofoccurrence categoriesorlife-cyclestagesoftheinsect(adults,nymphs,and adults+nymphs)observedonplantscanenablefarmerstoimprove theirmonitoringofcommercialcrops,leadingtosafermanagement decisions.

Bönischetal.(2004)usedindicatorkrigingofinterpolationsoil

propertiesexpressedbycategoricaldata.However,thisapproach showsweaknessesifanyofthecategorieshasalowoccurrence ratio, leading to problems in the geostatistical interpolations. Recently,Yamamotoetal.(2012),inatheoreticalstudy, recom-mended the use of multiquadric equations to map categorical variables,emphasizingthisapproachismoreefﬁcientthan Geo-statistics.

Thus,duetotheneedtoimprovesamplingproceduresforthe ricestembugincommercialirrigatedricecropsandthehigher exploration and applicability of interpolation methods for cat-egorical variables, this studyaimed tomap the spatiotemporal distributionofricestembuginﬂoodedricecrop.Thisstudyisin linewithrecenteffortstounderstandthespatiotemporal distri-butionofricestembugtosupportthedevelopmentofaneffective samplingschemeandconsequentlytheIPMpracticeincommercial riceﬁelds.

Materialandmethods Studyarea

Thestudywasconductedinthe2010/11and2011/12seasons inacommercialrice productioncropofaLuvisol withan aver-ageslopeof4.8%andlocatedinItaqui,RioGrandedoSul,Brazil (29◦0956.52Sand56◦2920.06W).Thismunicipalityispartof the“Western Frontier” rice region,which is thelargest cereal-producingregioninBrazil,withabout321thousandhectaresand anaverageyieldof8327kgha−1 inthe2016/17season()(IRGA,

2018).Thepredominant regionalclimateis “Cfa”,a subtropical,

warm temperate climate withwell-distributed rains and well-deﬁnedseasons,accordingtotheKöppen–Geigerclassiﬁcation.

Inbothseasons,thecropwasplantedviaminimaltillageby sowingthericecultivar“IRGA417”inthefirstweekofOctober, atadensity of60seedsperlinearmeterand spacingof0.17m betweenrows.Fertilization(N–P–K)consistedoftheapplicationof 286kgha−1of4–17–27atsowingtime,150kgha−1of45–0–0,15 daysafterseedlingemergence(beforefloodingthericepaddy),and 75kgha−1of30–0–20atthedifferentiationofthefloralprimordia stage.Thephytosanitarymanagementwasperformedaccording to thetechnical recommendations for irrigated rice cultivation

(Reunião, 2010),butwithnoinsecticideapplication.Intheﬁrst

season,duringricepost-harvestinmid-February,thecropwas sub-jectedtotwoplowingsandonelevelingharrowtodestroycrop residues.Inthe2011/12season,cropresiduesweredestroyedwith akniferoller.

Thephysiognomyofthebackgroundvegetationandother ele-mentsthatcomposedthelandscapeincludeaneucalyptusforeston thesouthernborder;aroadforcirculationandacorridorforcattle ﬂowonthenorth;ahighpresenceofspontaneousplants, predomi-nantlyApiaceae,Asteraceae,Cyperaceae,andPoaceaeonthewest; alocalaccessroadwithasmallextensionofaneucalyptusforest andahighincidenceofplantssimilartothosealreadymentioned attheeast.

Ricestembugmonitoring

TomonitorT.limbativentrisinthecropinbothseasons,aregular gridwithequidistantgeoreferencedsamplingpointswas previ-ously established as in Kuno (1991). The monitoring included biweeklysamplingsduringthevegetativeandreproductive phe-nologicalstagesofthericeplants(V4toR9)(Counceetal.,2000),

aswellassamplingsduringthepost-harvestbecausetheinsect canbefoundinthecropresidues(Bottaetal.,2014a).Inboth sea-sons,thespacingbetweensamplingpointswas10m,totaling693 samplingpointsin2010/11and352samplingpointsin2011/12. Ametalsquareof0.5×0.5mwasplacedoneachsamplingpoint, andtheplantsinsertedinthissquarewerevisuallyexaminedfor fouroccurrencecategories:(I)non-occurrenceof theinsect,(II) presenceof adultsonly,(III)presenceof nymphsonly,and (IV) coexistenceofbothphases.

Analysisandinterpolation

Anindicatorvariableforeachoccurrencecategorywascreated toindicateitschanceofoccurrenceornon-occurrenceinacertain region(samplingpointinthecrop).Thisvariableassumedvalues of0or1,representingitsabsenceorpresenceatthesamplingdate, respectively(Bönischetal.,2004;Yamamotoetal.,2012).

Afterobtainingtheindicatorvariable,thefrequency of each categorywasobservedatdifferentsamplingdates(phenological stagesofriceplants).Subsequently,thesymmetrytestwas per-formedtoverifywhetherthefrequenciesofoccurrencecategories weresimilarateachsamplingdate,twototwo,inbothseasons. Thesymmetrytest(p<0.05)wereperformedusingthepackage “rcompanion”ofRsoftware(RDevelopmentCoreTeam,2018).

The interpolation of occurrence categories of the rice stem bugwascarriedoutbymultiquadricequations(Yamamotoetal., 2012).Themultiquadricequationswereusedtointerpolatea non-sampledpointbymeansofalinearcombination,whoseweights wereobtainedbysolvingasystemoflinearequations.This sys-temofequationsusedaradialbasisfunctionofdistancesbetween sampledpointsand pointstobeestimated,andtheconsidered radialbasis functionwasthegeneralized multiquadric function

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Table1

FrequenciesofcategoriesofthericestembugTibracalimbativentris(countandpercentage)andsymmetrytestsappliedtothecomparisonbetweensamplingdates (phenologicalstages)inﬂoodedricecropinSouthernBrazil,2010/11cropseason.

Samplingdates(phenologicalstageb₎ _Categories

Ia _II _III _IV 12/13/10(V8)a Count(n) 532 52 101 8 Percentage(%) 76.77 7.50 14.57 1.15 12/27/10(V10/V11)b Count(n) 482 17 188 6 Percentage(%) 69.55 2.45 27.13 0.87 01/18/11(R1)c Count(n) 322 115 148 108 Percentage(%) 46.46 16.59 21.36 15.58 02/12/11(R9)d Count(n) 246 143 174 130 Percentage(%) 35.50 20.63 25.11 18.76 02/15/11(P.h.c₎_a Count(n) 525 32 120 16 Percentage(%) 75.76 04.62 17.32 02.31 Averagepercentage(%) 60.81 10.36 21.10 7.73

Samplingdatesfollowedbydifferentlowercaselettersdiffersigniﬁcantlybysymmetrytest(p<0.05).

a_Occurrence_categories_of_rice_stem_bug₌_I_–_no_insect,_II_–_adult,_III_–_nymphs,_and_IV_–_adult₊_nymphs. b_Phenological_stage_according_to_Counce_et_al.₍₂₀₀₀₎_.

c _Rice_stem_bug_sampling_in_{post-harvest.}_Crop_residues_not_destroyed.

The interpolation bymultiquadric equations wasperformed withGeovisual5.0softwareusinganalgorithmthatestimatedthe typeofoccurrenceofthericestembugatanon-sampledpointand selectedthatwiththehighestprobabilityofoccurrence (probabil-ityhigherthanorequalto72%)fromtheestimatedprobabilitiesfor eachtypeofcategoricalvariable(YamamotoandLandim,2013).In additiontothespatialinterpolationofoccurrencecategoriesofthe ricestembug,theuncertaintyassociatedwiththeinterpolation wasalsoestimated(YamamotoandLandim,2013).

Resultsanddiscussion

Inthe2010/11season,onaverage,T.limbativentrisdidnotoccur in60.81%ofthesampledpoints.Thepresenceofadults,nymphs, andbothphasesoccurredin10.36,21.10,and7.73%ofthesampled points,respectively(Table1).Inthe2011/12season,onaverage,the ricestembugdidnotoccurin73.01%ofthesampledpoints,while thepresenceofadults,nymphs,andbothphasesoccurredin12.22, 11.08,and3.69%ofthesampledpoints,respectively(Table2).These resultsweresimilartothoseobtainedbyAlvesetal.(2016),who reportedthenon-occurrenceofricestembugin67.78%ofthe sam-plingpointsdistributedinthecrops,aswellastheoccurrenceof adults,nymphs,andboth(adults+nymphs)in14.40,14.59,and 3.23%ofthesamplingpoints,respectively.

Thesymmetrytest forboth seasonsshoweddifferent occur-renceratesofT.limbativentrisatdifferentphenologicalstagesin whichsamplesweretaken.Whencomparingthesamplingdates, distinct counting behaviorsof each occurrence category of the insectwereobservedinbothseasons,exceptforthedatesof12/13 and 02/15in the2010/11and01/07 and01/21 in the2011/12 season,notdifferingsigniﬁcantly(Tables1and2).

Thevariability ateach occurrencecategory of ricestem bug atthedifferentsamplingdatesindicatesanassociationbetween occurrencecategoriesandthephenologicalstages,withthe phe-nologicalstagesofthericeanimportantfactorforinsectprevalence andricedamage(Hickeletal.,2016;KrinskiandFoerster,2017). Thespatiotemporalvariabilityofeconomicallyimportant arthro-podsinagriculturehasbeenreportedasstronglyrelatedtothe phenologicalstagesofcrops(Navaetal.,2018).Theoccurrenceof

T.limbativentrishasbeenreportedinriceﬁeldswhenplantsreach agrowthlevelsuitableforfeeding,whichoccursfromtheV4stage

andincreasesrapidlyasgenerationsdevelop,withahigher occur-rencefromthebeginningoftillering(V4)toﬂowering(R4),anda

reductioninthepost-harvest(Pazinietal.,2015a).

Thethematicmappingofthespatiotemporalbehaviorof occur-rencecategoriesofthericestembugincommercialﬂoodedricein twoagriculturalseasonsobtainedbymeansofmultiquadric equa-tionsisinFigs.1and2.Thereducedzonesofuncertaintyassociated withthesemappingaccuratelydeterminedthespatiotemporal dis-tributionoftheoccurrencecategoriesofinsectinthericeﬁelds.

Atthesamplingdatesof12/13inthe2010/11season(Fig.1A) and 11/19,12/03,and12/17 inthe2011/12season(Fig.2A–C), whichcorrespondtothestagesfromV4toV8/V9,apredominance

ofthecategoryI(non-occurrenceofinsects),inmorethan75%of thesampledpointswasobservedinthericepaddy.Initially,the ricestembugpopulationislow,resultingonlyfromthemigration ofpartofthepost-hibernatingpopulationsincethetotal abandon-mentofthewinterrefugessurroundingthecropcanbeextendedto January,dependingonbioticandabioticfactors(Bottaetal.,2014a). TheincidenceofcategoryII,composedonlyofT. limbativen-tris adults, occurredat the beginning of tillering of rice plants in marginal cropareas (edges) (Fig.2A–C) bythe migration of post-hibernating adults from adjacent vegetation, where they remainin theoff-season(Costaand Link,1992).Aphotoperiod higherthan12handtemperatureshigherthan22◦C determine theabandonment ofhibernation sites,migration torice plants, andconsequentstembugproliferationinricecrops(Bottaetal.,

2014a).Landscapecharacteristics,withthepresenceofplantsof

theApiaceae,Asteraceae,Cyperaceae,andPoaceaefamilies,which arepreferredhibernationrefugesforthericestembug(Bottaetal.,

2014b;Hickeletal.,2016)intheareassurroundingthestudied

riceﬁelds,thelowinnatemovementcapacityofpost-hibernating adults,thegreatneedtofeedonthealreadyformedstems,and matingpartnersmayexplain theirhigherconcentrationsat the cropedges.Monitoringofdifferentstinkbugspecies(Hemiptera: Pentatomidae)in differentagriculturalcropsfoundhigher den-sitiesinsamplesnearthecropedges,withasigniﬁcanteffecton spatiotemporal behavior of insects (“edge effects”) (Espino and

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Table2

FrequenciesofcategoriesofthericestembugTibracalimbativentris(countandpercentage)andsymmetrytestappliedtothecomparisonbetweensamplingdates(phenological stages)inﬂoodedricecropinSouthernBrazil,2011/12cropseason.

Samplingdates(phenologicalstageb₎ _Categories

Ia _II _III _IV 11/19/11(V4)a Count(n) 337 15 0 0 Percentage(%) 95.74 4.26 0.00 0.00 12/03/11(V6)b Count(n) 313 39 0 0 Percentage(%) 88.92 11.08 0.00 0.00 12/17/11(V8/V9)c Count(n) 280 69 3 0 Percentage(%) 79.54 19.60 0.85 0.00 01/07/12(V11)d Count(n) 214 13 114 11 Percentage(%) 60.79 3.69 32.39 3.12 01/21/12(R1)d Count(n) 205 9 116 22 Percentage(%) 58.24 2.56 32.95 6.25 02/02/12(R5)e Count(n) 170 103 28 51 Percentage(%) 48.29 29.26 7.95 14.49 02/15/12(R9)f Count(n) 188 95 49 20 Percentage(%) 53.41 26.99 13.92 5.68 02/29/12(P.h.c₎_g Count(n) 349 1 2 0 Percentage(%) 99.15 0.28 0.57 0.00 Averagepercentage(%) 73.01 12.22 11.08 3.69

Samplingdatesfollowedbydifferentlowercaselettersdiffersigniﬁcantlybysymmetrytest(p<0.05).

a_Occurrence_categories_of_rice_stem_bug₌_I_–_no_insect,_II_–_adult,_III_–_nymphs,_and_IV_–_adult₊_nymphs. b _Phenological_stage_according_to_Counce_et_al.₍₂₀₀₀₎_.

c _Rice_stem_bug_sampling_in_{post-harvest.}_Crop_residues_destroyed.

Way,2008;Tillmanetal.,2009;Reay-Jonesetal.,2010;Macfadyen

andMuller,2013;Pilkayetal.,2015;Venugopaletal.,2014,2015;

NguyenandNansen,2018;Pasinietal.,2018).

Theknowledgethatpost-hibernatingadultsofT.limbativentris, whichinitiatericecolonizationatthebeginningofplanttillering, areconcentratedspatiotemporallyinthemarginalextensionofthe cropinﬂuencedbytheedgehasseveralapplicationsinIPM.The resultsindicatethatsamplingeffortsofT.limbativentrisshouldbe concentratedattheentranceareasoftheinsect,startingfromthe riceﬁeldedgesatthebeginningofthetilleringperiod(Pazinietal.,

2015a).Thedevelopmentofpestmonitoringplansstratiﬁedand

directedalongthericeﬁeldedgesfromplanttilleringshouldbe consideredtoincreasetheefﬁciencyandreducesamplingefforts

(NguyenandNansen,2018).

Inaddition,itoptimizestheeffectiveuseoflocalizedcontrol measures(Barrigossietal.,2001),suchasinsecticidesprayingson theedgeextensionofthecrop,wherethepestisconcentratedatthe beginningandﬁrsthalfoftillering(Reay-Jonesetal.,2009;Toews

andShurley,2009;Venugopaletal.,2014).Thedirectedspraying

ofinsecticidesisaneffectivestrategytocontrolagriculturalpests, helpingtoreducetheproductioncostsandrisksofcontaminationin theagroecosystembysigniﬁcantlyreducingtheinsecticideamount

(NguyenandNansen,2018)comparedtoconventionalsprayings

scheduledthroughout thecrop, asusuallyemployed for T. lim-bativentrisinsouthernBrazil(Martinset al.,2016).Becausethe plantsare25–40cmhighandhavesparseleavesuntilmid-tillering, theprobabilityofthesprayedinsecticidereachingthestembugs betweenricestemsishigh(Meusetal.,2012).Thechemicalcontrol carriedoutduringthisperiodwouldsigniﬁcantlyeliminatetherice

stembugsbeforethebeginningoftheirreproductiveactivityand oviposition,avoidingarapidpopulationgrowth.

Nymphsonly(III)were predominantlyveriﬁedin upto33% ofthesamplingpointsbetweentheendofthevegetativestage (V10 and V11) and the beginning of the reproductive period

(R1) (Figs. 1Band 2D, E). These nymphs originated from

post-hibernatingindividualsandrepresenttheﬁrstsummergeneration of the rice stem bug in the crop. The thematic maps showed thebeginningoftheincidenceofthiscategoryremainsatsmall aggregationsneartheoccurrenceareasofpost-hibernatingadults

(Figs.1Aand2C).Ferreiraetal.(1997)pointedoutthatﬁrstinstar

nymphsareusuallygroupedaroundegg-massesandapparently do notfeed.However,fromthesecond instar,nymphsare less clusteredand presented moredispersionfor feeding,spreading spatially,asobservedinthisstudy(Figs.1Band2D,E).

Theoccurrence of thecategory IV (adults+nymphs), started markedlyat theR1 stage,butextendingtotheendof thecrop

cycleatstageR9,correspondingtothecompletematurityof

pan-iclegrains (Figs.1C, Dand 2E, F,G).In this period, thelowest indices of category I (non-occurrence of the insect) were also observed,indicatingthealmostabsolutecolonizationofthearea

(Tables1and2).Thehigherfrequencyofsamplingpointsonthe

mapswiththecoexistenceofadultsandnymphsfromthe begin-ningofthereproductivestageis causedbytheemergenceof a newpopulationofnymphsfromadultsoftheﬁrstsummer gen-eration,whichcharacterizesthesecondsummergenerationofthe ricestembug.In addition,this coexistenceindicatedthe occur-renceofoverlappinginsectgenerationsinthericecrop.Theadult populationofthesecondsummergenerationofT.limbativentris,

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Fig.1.InterpolationmapsbymultiquadricequationsofspatiotemporaldistributionofoccurrencecategoriesofTibracalimbativentris[I=noinsect(green),II=adult(red), III=nymphs(pink),IV=adult+nymphs(blue)]inﬂoodedricecropinSouthernBrazil,2010/2011cropseason.*Thematicmaps:(A)12/13/10[V8];(B)12/27/10[V10/V11];(C)

01/18/11[R1];(D)02/12/11[R9];(E)02/15/11[post-harvest=cropresiduesnotdestroyed].PhenologicalstageaccordingtoCounceetal.(2000).

whicharecomposedofthepre-hibernatingpopulation,hasalow potentialtodamagethecropsduetotheadvancedphenological cycleoftheplants.Thericestembugcanproduceuptothree gener-ationsinricecropsandthethirdisusuallycompleteincropresidues andplantsadjacenttothecropatthebeginningoftheoff-season

(Bottonetal.,1996;Ferreiraetal.,1997;Bottaetal.,2014a).

Thereductionofstembugpopulationwasonlydetectedin post-harvestsamples,withcategoryI(non-occurrenceoftheinsect)in morethan75%ofthesampledpoints(Tables1and2).The reduc-tionofthepost-harvestpopulation,detectedinthe2011/12season

(Table2,Fig.2H),wassigniﬁcantcomparedtothepreviousseason

(Table1,Fig.1E)mainlyduethemortalityorscapegeneratedbythe

destructionofcropresiduesbythekniferollerhoursaftertherice harvest.Thus,theanticipationofcropmanagementoperationsin post-harvestofcommercialriceﬁeldsmayhelptoreduced popula-tionofpre-hibernatingadults.Theincorporationofcropresiduesis

anefﬁcienttechniqueofmechanicalcontrolofinsectpestsin sev-eralcropsandavoidsfavorableconditionsofwinterrefugeforthe T.limbativentrispopulationduringtheoff-seasonofthericecrop

(Pazinietal.,2012).

In thecontext oftheIPM in Brazilian ricecrops, theresults obtainedinthis studyareanessentialandpioneeringapproach demonstrating the spatiotemporal distribution of T. limbativen-tris. With the recent advances in the knowledge about this pest population dynamics in rice agroecosystem (Botta et al.,

2014a; Pazini et al., 2015a, 2015b, 2015c, 2015d, 2017; Alves

et al., 2016), these studies can provide scientific bases for the development of efficient monitoring techniques and more environmentally correct pest management actions(site-specific management), reducing the production costs with emphasis on diminishing insecticide use that can cause environmental contamination.

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H

I II III IV N

Fig.2. InterpolationmapsbymultiquadricequationsofspatiotemporaldistributionofoccurrencecategoriesofTibracalimbativentris[I=noinsect(green),II=adult(red), III=nymphs(pink),IV=adult+nymphs(blue)]inﬂoodedricecropinSouthernBrazil,2011/2012cropseason.*Thematicmaps:(A)11/19/11[V4];(B)12/03/11[V6];(C)

12/17/11[V8/V9];(D)01/07/12[V11];(E)01/21/12[R1];(F)02/02/12[R5];(G)02/15/12[R9];(H)02/29/12[post-harvest=cropresiduesdestroyed].Phenologicalstage

accordingtoCounceetal.(2000).

Conclusions

Ina ricecrop, itcanbeexpectedthatmorethan 66%ofthe areawillhave norice stem bug. “Adults”of rice stem bug are the most abundant insect category until mid-vegetative phase of rice crop while “nymphs” are the most abundant from the endofthevegetativephase.Theadultcategorycompletely con-centrates at edge of the ﬁeld until mid-vegetative phase of the rice crop, which indicates that localized control measures couldbeusedtoeffectivelyeliminatethepestbeforepopulation growth.

Funding

Thisresearchdidnotreceiveanyspeciﬁcgrantfromfunding agenciesinthepublic,commercial,ornot-for-proﬁtsectors. Authorcontributionstatement

FFS,JFSM,andJAFBconceivedanddesignedtheresearch.JBP andHSCconductedtheexperiments.EJS,AMS,andHSCanalyzed data.HSCandJBPwrotethemanuscript.Allauthorscontributedin

(7)

revising and preparing the paper for submission. All authors approvedthemanuscript.

Conﬂictsofinterest

Theauthorsdeclarenoconﬂictsofinterest. Acknowledgments

Theauthors would like tothank theentomology laboratory membersatUNIPAMPA(LABENTO)fortheirsupportincarrying out this research.Special thanks toRobson AntônioBotta and RodrigoRübenichfortheirfullassistancesintheﬁeld.Wethank thePitangueiraRiceCompanyforsupplyingthericeﬁeldsforthis studyandtheirfullcourtesyandcooperationinthisresearch. References

Alves,T.M.,Maia,A.H.N.,Barrigossi,J.A.F.,2016.Spatialdistributionandcoexisting patternsofadultsandnymphsofTibracalimbativentris(Hemiptera: Pentatomi-dae)inpaddyriceﬁelds.Environ.Entomol.45(6),1505–1514.

Barrigossi,J.A.F.,Young,L.J.,Crawford,C.A.G.,Hein,G.L.,Leon,G.,Higley,L.G.,2001.

SpatialandprobabilitydistributionofMexicanbeanbeetle(Coleoptera: Coc-cinellidae)eggmasspopulationsindrybean.Environ.Entomol.30(2),244–253.

Bönisch,S.,LopesAssad,M.L.,Monteiro,A.M.V.,Câmara,G.,2004.Representac¸ãoe propagac¸ãodeincertezasemdadosdesolo.II-Atributosnuméricos.Rev.Bras. Ciênc.Solo.28(1),33–47.

Botta,R.A.,daSilva,F.F.,Pazini,J.B.,Martins,J.F.S.,Rübenich,R.,2014a. Abundân-ciasazonaldepercevejo-do-colmodoarroz.Pesqui.Agropecu.Trop.44(4), 417–423.

Botta,R.A.,Silva,F.F.,Pazini,J.B.,Rübenich,R.,2014b.EstratégiademanejodeTibraca limbativentrisStal(Hemiptera:Pentatomidae)naentressafradaculturadoarroz irrigado.Rev.Agric.89(3),224–231.

Botton,M.,Martins,J.F.S.,Loeck,A.,Rosenthal,M.A.,1996.BiologiadeTibraca lim-bativentrisStalsobreplantasdearroz.An.Soc.Entomol.Bras.25(1),21–26.

CONAB,2018.CompanhiaNacionaldeAbastecimento,2018.Acompanhamentode safrabrasileira:grãos,v.5–safra2017/18,oitavolevantamento,maio.Conab, Brasília,https://conab.gov.br/info-agro/safras/graos(accessed07.06.18). Costa,E.C.,Link,D.,1992.DispersãodeTibracalimbativentrisStal,1860(Hemiptera:

Pentatomidae)emarrozirrigado.An.Soc.Entomol.Bras.21(1),197–202.

Counce,P.A.,Keisling,C.,Mitchell,A.J.,2000.Auniform,objective,andadaptative systemforexpressingricedevelopment.CropSci.40(2),436–443.

Espino,L.,Way, M.O., 2008. Attractiveness ofstages of ricepanicle develop-menttoOebaluspugnax(Hemiptera:Pentatomidae).J.Econ.Entomol.101(4), 1233–1237.

FAOSTAT,2016.FoodandAgricultureOrganizationoftheUnitedNationsStatistical Database,https://www.fao.org/faostat/en/#rankings/countriesbycommodity

(accessed06.05.18).

Ferreira,E.,Zimmermann,F.J.P.,SantosA.B.dos,NevesB.P.das.,1997.O percevejo-do-colmonaculturadoarroz.Goiânia:EmbrapaArrozeFeijão (Documen-tos,75),https://www.infoteca.cnptia.embrapa.br/handle/doc/204293(accessed 05.05.18).

Hickel,E.R.,Prando,H.F.,Eberhardt,D.S.,2016.Percevejosnaslavourascatarinenses dearrozirrigado:ocorrência,monitoramentoemanejointegrado.Florianópolis: Epagri.(Boletim,173).

IRGA. Instituto RioGrandense doArroz, 2018. Produc¸ão municipal 2016/17,

https://stirga2018-admin.hml.rs.gov.br/upload/arquivos/201805/21164049-produtividade-municipios-safra-2016-e-2017-ﬁnal.pdf(accessed01.05.18). Krinski,D.,Foerster,L.A.,2017.DamagebyTibracalimbativentrisStål(Pentatomidae)

touplandricecultivatedinAmazonrainforestregion(Brazil)atdifferentgrowth stages.Neotrop.Entomol.46(1),107–114.

Kuno,E.,1991.Samplingandanalysisofinsectpopulations.Annu.Rev.Entomol.36, 285–304.

Macfadyen,S.,Muller,W.,2013.Edgesinagriculturallandscapes:species interac-tionsandmovementofnaturalenemies.PLoSOne8(3),e59659.

Martins,J.F.S.,Grützmacher,A.D.,Cunha,U.S.,2004.Descric¸ãoemanejointegrado deinseto-pragaemarrozirrigado.In:Gomes,A.,da,S.,MagalhãesJunior,A.M. (Eds.),ArrozIrrigadonoSuldoBrasil.EmbrapaInformac¸ãoTecnológica,Brasília, pp.635–676.

Martins, J.F.S., da Silva, F.F., Theisen, G., Mattos, M.L.T., Botta, R.A., Pazini, J.B., Nunes, C.D.M., 2016. Diagnóstico sobre o manejo de agrotóxicos em áreas orizícolas da Fronteira Oeste do Rio Grande do Sul. Embrapa

ClimaTemperado,Pelotas(Documentos,421).https://ainfo.cnptia.embrapa.br/ digital/bitstream/item/161942/1/Documento-421.pdf(accessed02.06.18). Meus,N.C.,Pazini,J.B.,Botta,R.A.,Dias,N.P.,Silva,F.F.,2012.Horadeaplicar.Cult.

Grand.Cult.13(151),36–38.

Nava,D.T.,Nicolis,O.,Uribe-Opazo,M.A.,BastianiF.de.,2018.Statisticalmethods foridentifyinganisotropyintheSpodopterafrugiperdaspatialdistribution.Span. J.Agric.Res.16(1),e1003.

Nguyen,H.D.D.,Nansen,C.,2018.Edge-biaseddistributionsofinsects.Areview. Agron.Sustain.Dev.38(11),1–13.

Panizzi,A.R.,2015.Growingproblemswithstinkbugs(Hemiptera:Heteroptera: Pentatomidae):speciesinvasivetotheU.S.andpotentialNeotropicalinvaders. Am.Entomol.61(4),223–233.

Pasini,M.P.B.,Lúcio,A.D.,CargneluttiFilho,A.,Ribeiro,A.L.P.,Zamberlan,J.F.,Lopes, S.J.,2018.PopulationdensityofTibracalimbativentrisonﬂoodirrigatedriceand alternativehostplants.Pesq.Agropec.Bras.53(3),265–278.

Pazini,J.,de,B.,Botta,R.A.,SilvaF.F.da.,2012.Mortalidadedepercevejo-do-colmo doarroznopreparodosoloparacultivomínimo.Pesq.Agropec.Bras.47(7), 1022–1024.

Pazini,J.,de,B.,Botta,R.A.,Seidel,E.J.,SilvaF.F.da,Martins,J.F.S.,Barrigossi,J.A.F., Rübenich,R.A.,2015a.Geoestatísticaaplicadaaoestudodadistribuic¸ãoespacial deTibracalimbativentrisemarrozalirrigadoporinundac¸ão.Cienc.Rural45(6), 1006–1012.

Pazini,J.B.,Seidel,E.J.,Silva,F.F.,Martins,J.F.S.,Barrigossi,J.A.F.,2015b. Dimen-sionamentoamostraldopercevejo-do-colmoTibracalimbativentrisStal,1860 (Hemiptera:Pentatomidae)emarrozirrigado.In:CongressoBrasileirodeArroz Irrigado,9,2015,Pelotas.Anais.Pelotas:EmbrapaClimaTemperado/SOSBAI, pp.1–4,https://www.cbai2015.com.br/docs/trab-4-4214-49-1506180048.pdf

(accessed22.06.18).

Pazini,J.B.,Seidel,E.J.,daSilva,F.F.,Botta,R.A.,Martins,J.F.S.,2015c.Malhasamostrais aplicadasaomapeamentodaprobabilidadedeocorrênciadeTibraca limbat-iventrisemarrozirrigado.In:SimpósiodeGeoestatísticaAplicadaemCiências Agrárias,4,2015,Botucatu.Anais.UNESP,Botucatu,pp.1–6.

Pazini,J.B.,Seidel,E.J.,daSilva,F.F.,Botta,R.A.,Martins,J.F.S.,2015d.Análise espa-cialmultivariadaaplicadaaomapeamentodaprobabilidadedeocorrênciado percevejo-do-colmoemarrozirrigado.In:SimpósiodeGeoestatísticaAplicada emCiênciasAgrárias,4,2015,Botucatu.Anais.UNESP,Botucatu,pp.1–6.

Pazini,J.B.,SeideL,E.J.,daSilva,F.F.,Barrigossi,J.A.F.,Martins,J.F.S.,Botta,R.A.,2017.

Spatialarrangementvalidationofthericestembuginﬂoodedriceﬁeld.Ciênc. Natura39(2),221–232.

Pias,O.H.D.C.,Cherubin,M.R.,Berghetti,J.,Kuss,C.C.,Santi,A.L.,Basso,C.J.,2017.

SamplinggridsformonitoringEuschistusherosinfestationinsoybean.Bragantia 76(3),386–397.

Pilkay,G.L.,Reay-Jones,F.P.,Toews,M.D.,Greene,J.K.,Bridges,W.C.,2015.Spatial andtemporaldynamicsofstinkbugsinsoutheasternfarmscapes.J.Insect.Sci. 15(23),1–13.

RDevelopmentCoreTeam,2018.R:ALanguageandEnvironmentfor Statisti-calComputing.Version.3.5.0.RFoundationforStatisticalComputing,Vienna,

https://r-project.org/(accessed19.03.18).

Reay-Jones,F.P.F.,Greene,J.K.,Toews,M.D.,Reeves,R.B.,2009.Samplingstinkbugs (Hemiptera:Pentatomidae)forpopulationestimationandpestmanagementin southeasterncottonproduction.J.Econ.Entomol.102(6),2360–2370.

Reay-Jones,F.P.F.,Toews,M.D.,Greene,J.K.,Reeves,R.B.,2010.Spatialdynamicsof stinkbugs(Hemiptera:Pentatomidae)andassociatedbollinjuryin Southeast-erncottonﬁelds.Environ.Entomol.39(3),956–969.

ReuniãoTécnicadaCulturadoArrozIrrigado,2010.Arrozirrigado:Recomendac¸ões técnicasdapesquisaparaoSuldoBrasil.SOSBAI,PortoAlegre.

ReuniãoTécnicadaCulturadoArrozIrrigado,2016.Arrozirrigado:Recomendac¸ões técnicasdapesquisaparaoSuldoBrasil.SOSBAI,Pelotas.

Tillman,P.G.,Northﬁeld,T.D.,Mizell,R.F.,Riddle,T.C.,2009.Spatiotemporal pat-ternsanddispersalofstinkbugs(Heteroptera:Pentatomidae)inpeanut-cotton farmscapes.Environ.Entomol.38(4),1038–1052.

Toews,M.D.,Shurley,W.D.,2009.Cropjuxtapositionaffectscottonﬁberqualityin Georgiafarmscapes.J.Econ.Entomol.102(4),1515–1522.

Toledo,F.,Barbosa,J.C.,Yamamoto,P.T.,2006.Distribuic¸ãoespacialdeToxoptera citricida(Kirkaldy)(Hemiptera:Aphididae)naculturadecitros.Rev.Bras.Frutic. 28(2),194–198.

Venugopal,P.D.,Coffey,P.L.,Dively,G.P.,Lamp,W.O.,2014.Adjacenthabitat inﬂu-enceonstinkbug(Hemiptera:Pentatomidae)densitiesandtheassociated damageatﬁeldcornandsoybeanedges.PLoSOne9(10),e109917.

Venugopal,P.D.,Martinson,H.M.,Bergmann,E.J.,Shrewsbury,P.M.,Raupp,M.J., 2015.EdgeeffectsinﬂuencetheabundanceoftheinvasiveHalyomorphahalys (Hemiptera:Pentatomidae)inwoodyplantnurseries.Environ.Entomol.44(3), 474–479.

Yamamoto,J.K.,Landim,P.M.B.,2013.Geoestatística:conceitoseaplicac¸ões.Oﬁcina deTextos,SãoPaulo.

Yamamoto,J.K.,Mao,X.M.,Koike,K.,Crosta,A.P.,Landim,P.M.B.,Hu,H.Z.,Wang, C.Y.,Yao,L.Q.,2012.Mappinganuncertaintyzonebetweeninterpolatedtypes ofacategoricalvariable.Comput.Geosci.40(1),146–152.