What have we learned from the dead? A compilation of three years of cooperation between entomologists and crime scene investigators 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

What

have

we

learned

from

the

dead?

A

compilation

of

three

years

of

cooperation

between

entomologists

and

crime

scene

investigators

in

Southern

Brazil

Rodrigo

C. Corrêa

a,∗

_,

_Maria

_F.C.

_Caneparo

a

_,

_Karine

_P.

_Vairo

a

_,

_Alexandre

_G.

_de

_Lara

b

_,

Mauricio

O. Moura

a

a_Universidade_Federal_do_Paraná,_Departamento_de_Zoologia,_Curitiba,_PR,_Brazil b_Instituto_de_{Criminalística}_do_Paraná,_Curitiba,_PR,_Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received16January2019 Accepted27May2019 Availableonline15June2019 AssociateEditor:RodrigoKruger Keywords: Cases Coleoptera Diptera Forensicentomology PMI

a

b

s

t

r

a

c

t

Withhomiciderateshigherthantheworldaverage,Brazilstandsoutasoneofthemostviolentcountries worldwide.Timeofdeathestimationbasedsolelyonbodychangescanbebiasedorinaccurate; foren-sicentomologycanplayadeterminantroleinsuchcases.Accurateknowledgeofnecrophilousfaunais essentialtovalidateexperimentaldataandallowsfortheapplicationofentomologicalevidencein foren-sicinvestigations,whichbenefitsscientists,investigators,andsocietyingeneral.Entomologicalevidence fromCuritibaand22nearbycitieswerecollectedbycrimesceneinvestigatorsfromtheScientificPolice ofParaná.Thecorpseswerefoundindiverseenvironmentsandspecimensfromeachspecieswere col-lectedfromalllifestages.Wepresentdatafrom25casesfrom2011to2014,includingassociatedspecies, newrecords,andcomparisonsbetweenexistingexperimentaldataanddatafromspeciescollectedin thecasespresented.Weidentified23totalspecies,ofwhicheightspeciesofColeopteraandtwospecies ofDipterahavenotpreviouslybeenrecordedoncorpses.Inallcases,Calliphoridae(76%)andSilphidae (48%)werethemostnumerousfamiliescollected.Workingtogetherwiththescientificpolicegaveus insightintowhichspecieslackeddetailedrecordsandenabledustocollaborativelyfocusonresolving deficitsinourknowledgeofnecrophagousinsects.

Introduction

Forensicentomologyisknownastheuseofinsectsandother arthropodsasevidenceinlegalcases(CattsandGoff,1992).When insectspecimensarecollectedfromadeathscene,thepostmortem interval(PMI),ortimeelapsedbetweendeathanddiscoveryofthe body,canbeestimatedbyevaluatingtheperiodinsectactivityon thecorpse(Tomberlinetal.,2011).Theapplicationofthisscienceis heavilydependentonavailableknowledgeofnecrophilousspecies, suchastaxonomy,biology,behavior,ecology,andsuccessional pat-tern(e.g.ByrdandCastner,2010;Smith,1986).

Historically,theﬁrstforensicentomologypublicationsinBrazil datefromtheearly1900s(Freire,1914a,1914b;Roquete-Pinto, 1908).However,basicresearchformallystartedinthelatenineties with Souza and Linhares (1997) and Moura et al. (1997) pre-sentinginformationaboutsuccessionalpatternsofnecrophagous

∗ Correspondingauthor.

E-mail:r.ccorrea@yahoo.com(R.C.Corrêa).

speciesofpotentialforensicinterest.Themedico-legalapplication offorensicentomologyhasproducedfewcasereportssincethen (Kosmannetal.,2011;Oliveira-CostaandLopes,1999; Oliveira-CostaandMello-Patiu,2004;Pujol-Luzetal.,2006,2008a;Souza etal.,2014;Vairoetal.,2015b,2017;Vasconcelosetal.,2014).The smallnumberofcasereportscanbeattributedinparttothelack ofcollaborationbetweenacademia(i.e.universitiesandresearch centers)andBrazilianlawenforcementagencies(Pujol-Luzetal., 2008b).

Brazilistheﬁfthlargestcountryintheworldwithremarkable faunaanda complexarrayofbiomes.Thenumber ofidentiﬁed insect species is around 90,000,but is estimated to bearound 400,000(Rafaeletal.,2012).Therefore, surveysinallecological regionsofthecountryareofcriticalimportancetoassessspecies ofpotentialforensicinterestanddirectstudiestoallowtheuse of relevant species in investigations. The review presented by

Pujol-Luzetal.(2008b)mentionedtheneedofregionaldatabases, whileOliveiraandVasconcelos(2010)andVasconcelosandAraujo (2012)addressedthestateofartinNortheastregion.Nevertheless,

https://doi.org/10.1016/j.rbe.2019.05.009

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Brazilianforensicentomologistsfaceamajorissue:thelackof avail-abledataforPMIestimation.

Itis wellknownthatBrazilhashighrates ofviolentcrimes. Accordingtorecentreports,Brazilianhomicideratesarefourtimes higherthan theworldaverage(Butchart, 2014).In somecases, homicideinvestigationscanbecompromisedbyuncertaintiesin PMIestimation.Forensicentomologyhasthepotentialtoprovide decisiveinputintheseinstances.However,recordeddata regard-ingthediversityofnecrophilousfaunaisusuallyrestrictedtothe resultsofexperimentswithanimal models.Thus,thevalidation ofexperimentaldataisnecessary toreliably makeuseof ento-mologicalevidence.Thereisnodoubtthatcollaborationsbetween scientistsandinvestigatorsbeneﬁtbothsides.

Themainobjectiveofthispaperistopresenttheresultsofthe collaborationbetweenParanáStateScientiﬁcPoliceandthe Fed-eralUniversityofParaná(UniversidadeFederaldoParaná–UFPR). Wepresentdatafrom25casesbetween2011and2014,including associatedspecies,newrecords,andcomparisonbetween experi-mentaldataandthespeciesfoundoncorpses.Withourresults,we expecttocontributetotheimprovementofthelocaldatabaseof necrophilousinsectsandBrazilianforensicentomology.

Materialandmethods

Locality

Paraná(199.307,945km2₎_is_a_state_located_in_Southern_Brazil

withestimatedpopulationof11,163.018in2015(IBGE,2015).The climateisdividedinthreetypesincludingtropicalandsubtropical withvariationsontemperatureandrain(Af,CfaandCfbonKoppen classiﬁcation).Thecapital,Curitiba,hasthelargestpopulationin SouthernBrazilandistheeighthmostpopulatedcityinthecountry withover1.8millionpeople(IBGE,2015).Themetropolitanarea comprisesof26citiesandover3.2millioninhabitants(Prefeitura MunicipaldeCuritiba,2015).

CuritibahasbeenoneofthemostdangerouscitiesinSouthern Brazilforthepast6years(SESP-PR,2015;SSP-RS,2015;SSP-SC, 2015),and hasbeenthemostviolentcityinParanásince2011 (SESP-PR, 2015).Accordingtogovernment reports, therates of homicide(343),robberyfollowedbydeath(22),andinjury result-ingdeath(5)inCuritibawereatleastfourtimeshigherthanthe secondhighestrankedcityin2015(SESP-PR,2015).

Datacollection

Entomologicalevidencefrom25deathinvestigationswere col-lectedbycrimesceneinvestigators fromParanáStateScientific Police(PolíciaCientíficadoParaná)between2011and2014. Spec-imensandmaterialscollectedfromthedeathscenesweresentto theUFPRForensicEntomologyGroupforrearingandidentification. Casedatawastakenfrom11citiesunderthejurisdictionof Scien-tificPoliceinvestigators(Fig.1),whichincludesCuritibaand22of itssurroundingcities(SESP-PR,2015).

Thecorpseswerefoundindiverseenvironmentsincludingrural and urban, and indoor and outdoorlocations. Data from cases includemunicipality,geographical coordinates,habitat(rural or urban),ambient(indoororoutdoor),speciescollected,and devel-opmentalstage(egg,larvae,pupae,oradult).

Toevaluatetherelativepresenceofspeciesandfamiliesineach case, we calculated theproportion (or relative frequency). The proportion(P)isthenumberofobservations(NO)ofacategory (species/family)dividedbythetotalnumberofobservations(TO) multipliedby100.

P=

NO TO

×100.

Speciesidentiﬁcationandrearingprocedures

Asastandardprocedure,around30%oftheimmature speci-mens(eggs,maggots,larvae,andpupae)collectedwereﬁxedand preservedin70%alcohol.Theremainingspecimenswerereared in ground beef under controlled conditions (25◦C, 70% RH) to adulthood.Adultspecimenscollectedwerepinnedandidentiﬁed usingtheavailableliterature(e.g.CarvalhoandMello-Patiu,2008; Navarrete-Herediaetal.,2002;Vairoetal.,2011,2015a)and con-sultingspecialists.

AllspecimensreceivedweredepositedatPadreJesusSantiago MoureEntomologicalCollection(DZUP)atUFPR.

Results

Generaldescriptionofcasesandentomologicalevidence

The corpses were found in diverse environments including rural/urban, indoor/outdoor locations.We compilated all infor-mation datain a tablethat includes municipality,geographical coordinates,habitat(ruralorurban),ambient(indoororoutdoor), speciescollected,anddevelopmentalstage(egg,larvae,pupae,or adult)(Table1).Mostcaseswereinrural(72%)andoutdoor(76%) areas.Itisimportanttonotethatallurbancases,withone excep-tion,wereindoor.Nine(36%)caseswerelocatedinCuritiba,with casessplit55:45urbantoruraland55:45outdoortoindoor.Four ofthesixindoorcasesreviewedwereinCuritiba.

Twenty-six insect species from ten families were collected (Table 2). Eleven species of Coleoptera belonging to ﬁve familieswererecorded:Dermestesmaculatus(DeGeer,1774), Der-mestesperuvianusLaporte,1840(Dermestidae),Euspilotusazureus (Sahlberg, 1823), Hister cavifrons Marseul, 1854 (Histeridae), Pelossomaaff.laferteiMulsant,1844(Hydrophilidae),Oxelytrum dis-cicolle(Brullé,1840),Oxelytrumerythrurum(Blanchard,1840) (Sil-phidae),AleocharapseudochrysorrhoaCaron,Mise,Klimaszewski, 2008,CreophilusvariegatusMannerheim,1830,Philonthus hepati-cusErichson,1840,Philonthussp.(Staphylinidae).Fifteenspecies of Diptera from ﬁve families were recorded: Chrysomya albi-ceps(Wiedermann,1819),Chrysomyaputoria(Wiedermann,1830), Cochliomyiamacellaria(Fabricius,1975),Hemiluciliasemidiaphana (Rondani,1850),Luciliaeximia(Wiedmann,1819),Luciliasericata (Meigen,1826),Paraluciliapseudolyrcea(Mello,1969)(=Paralucilia xanthogeneiatesDear1985),Sarconesiachlorogaster(Wiedemann, 1830),Calliphoridaesp.(Calliphoridae),MuscadomesticaLinnaeus, 1758,Ophyraaenensis(Wiedemann,1830) (Muscidae),Phoridae sp.(Phoridae),Piophilacasei(Linnaeus,1758)(Piophilidae), Micro-cerellahalli(Engel,1931),Peckia(Pattonella)resona(Lopes,1935) (Sarcophagidae).

Amongtheforensicallyrelevantfamilies, Calliphoridae(76%) andSilphidae(48%)werethemostfrequentlyencounteredatthe deathscenes.The mostrecurrent species wereO. discicolle(11 cases),C.albiceps(10cases),H.semidiaphana(6cases),andP. pseu-dolyrcea(5cases).Calliphoridae(9)andStaphylinidae(4)werethe richestfamiliesintermsofthenumberofidentiﬁedspecies.

Forcomparisonpurposes,regionaldatagatheredfrom previ-ouscarrionecologystudiesandauthorsthatcollectedthespecies observedarelistedinTable3.Onthistable,onlyspecimens iden-tiﬁed at species level are present. Coleoptera had ten species collectedonpreviousexperiments; however, only D. maculatus haspreviousrecordsonhumanbodies.ForDiptera,elevenspecies werecollectedonpreviousexperiments,andtwelvespecieswere recorded in case studies or collected on corpses. Considering specieswithknownforensicimportance(i.e.reportedincase stud-iesorcollectedonhumanbodies),ourresultsincludetenspecies withoutpreviousrecordinforensicstudies,eightinColeopteraand

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1 2 3 4 5 6 7 8 9 10 11

Fig.1.LocationofParanáState(SouthernBrazil)andmunicipalitieswherethecasesoccurredindetail.(1)PontaGrossa,(2)CampoMagro,(3)Colombo,(4)CampinaGrande doSul,(5)QuatroBarras,(6)Curitiba,(7)SãoJosédosPinhais,(8)FazendaRioGrande,(9)Araucária,(10)CampodoTenente,(11)Lapa.

twoinDiptera.Detailedinformationwithallspeciescollectedin regionalstudiesisavailableinthesupplementarymaterial.

Discussion

Forensic entomological experimental methodology assumes thatfaunafoundonanimalremainsandhumanremainsare simi-lar.Duetherestrictionsontheexperimentaluseofhumanbodies (mostlymoral,ethical,orreligious),surveysusinganimalmodelsor baitsarethestandardprocedure(seeCattsandGoff,1992;El-Kady, 1999).Studieswithanimalmodelscanprovideanideaofspecies presentinaspeciﬁcregionbeforeactualapplicationinforensic entomologycases.Evenwiththepossibilityofoverestimation, sur-veyresults(OliveiraandVasconcelos,2010)stillplayasigniﬁcant roleasadatabaseofspeciesofpotentialimportanceinforensic entomology.

Fromthe23speciescollectedfromthecasesreviewed,17(68%) had previous records in regional literature and 12 (48%) were recordedinstudieswithhumanbodiesinBrazil(Table3).Dermestes peruvianus,P.lafertei,C.variegatus.P.hepaticus,C.macellaria,and P.caseiwerenotcollectedinpreviousexperiments.Globally,asin Brazil,mostpublishedcasesconcerningforensicentomologyare focusedonDiptera.Asaresult,90%ofColeopteraspeciescollected aspartofforensicinvestigationsorstudiesdonothavepreviously recordedinteractionswithhumanbodies.

Coleopterahasseveralspecieswithrelevancetoforensic ento-mology(e.g.ÖzdemirandSert,2009;PayneandKing,1970;Smith, 1986).However,theforensicimpactofColeopteraisfrequently underestimatedduetotaxonomicdifﬁcultiesand alackof eco-logicalandbehavioralknowledge(Almeidaetal.,2015).Although multiplesurveyshavebeenperformedintheCuritibaarea,four speciesnotedinthisinvestigationhaveneverbeennotedonhuman bodiesinthisregion,andonlyD.maculatusandO.discicollehave previouslybeennotedonhumanbodiesinBrazil.Theresultsofthis studydemonstratethatrelianceonexistingexperimentaldatacan leadtounderestimationoftherangeoffaunafoundoncorpses.

Silphidaewaspresenton12cases(48%),representedbythe genusOxelytrum.Adultsofthis genusareomnivorousand both feedonthecorpseandpreyonmaggots,whilelarvaearepurely necrophagous(Olivaand diLorio,2008).Despite beingthe sec-ondmostabundantfamilyafterCalliphoridae(Diptera),thereare norecordsofO.erythrurumorO.discicollebeingassociatedwith humanbodiesinBrazil(seeAlmeidaetal.,2015).Inthreecases (Table1–cases7,20,23),O.discicollewascollectedatlarvalstage andwastheprimaryspeciesforPMIestimation.Thenecrophagous habitoflarvae,presenceduringinitialstagesofdecomposition,and highsamplingincasesinthepresentstudyhighlightsthe impor-tanceofOxelytrumspeciesandtheirbiologicaldata.

Dermestidaeisoneofthemostimportantfamiliesassociated withcarcasses,corpses,and storedproducts(Byrdand Castner, 2010).Charabidzeetal.(2013)gatheredinformationpertainingto Dermestespresenceon81forensiccasesandfoundD.maculatus presenton7.4%ofcasesandD.peruvianuspresenton12.3%ofcases. Amongthe25casesevaluatedinthepresentstudy,Dermestidae wasrepresentedin12%ofcases,withD.maculatuspresentin8%of casesandD.peruvianuspresentin4%ofcases.Bothspecieswere collectedinindoorlocations,D.maculatusaslarvalspecimens(Case 24)andD.peruvianusasadultspecimens(Case4)(seeTable1). OurresultsareconsistentwithCharabidzeetal.(2013)withmost recordsforindoorcases.Duetheirstatusasurbanpests,speciesof Dermestidaetendtobemorerelatedwithurbanareasthanother forensicallyrelevantColeopteraandaremorelikelytobefound inindoordeathscenes.Priortothisinvestigation,D.peruvianusis onlymentionedinaforensiccontextinSouzaandLinhares(1997)

studywithpigcarrion,inwhichthepresenceofD.maculatuswas alsonoted.

ThereisnoliteratureconcerningP.laferteibiologyorbehavior. AccordingtoForbesandDadour(2010),specimensbelongingtothe samefamilycanbeobservedfeedingoneggsandmaggotsduring theﬁrststagesofdecompositionofpigcarcasses.Hydrophilidae, mostlyinregardstoSphaeridinae,asemi-aquaticspecies,isa fam-ilywithpotentialforensicimportancethatshouldbedetermined

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Table1

Generalviewofthecases.Municipalitieswerethecorpseswerefound,habitat(ruralorurban),ambient(outdoororindoor),andspeciescollectedoneachcase.(E)egg,(L) larvae,(P)pupae,(A)adult.

Case Municipality(coordinates) Habitat Ambient Species

1 Colombo(−25.354811,

−49.140069)

Rural Outdoor Hemiluciliasemidiaphana(L),Muscadomestica(A)

2 Curitiba(−25.568583,

−49.315025)

Rural Outdoor Chrysomyaalbiceps(E),Paraluciliapseudolyrcea(E)

3 SãoJosédosPinhais

(−25.700039,−49.099119)

Rural Outdoor Histercavifrons(A),Oxelytrumdiscicolle(A),Pelosomaaff.

lafetertei(A),Philonthussp.(A)

4 Curitiba(−25.426317,

−49.280983)

Urban Indoor Chrysomyaalbiceps(L),Dermestesperuvianus(A)

5 CampinaGrandedoSul

(−25.25427,−48.9179)

Rural Outdoor Oxelytrumdiscicolle(A),Sarconesiachlorogaster(A)

6 Curitiba(−25.547053,

−49.25295)

Urban Indoor Chrysomyaalbiceps(E/L),Hemiluciliasemidiaphana(E/L),

Luciliasericata(E/L),Sarconesiachlorogaster(P)

7 CampodoTenente

(−25.91785,−49.603281)

Rural Outdoor Chrysomyaalbiceps(A),Ophyraaenensis(A),Oxelytrum

discicolle(L),Paraluciliapseudolyrcea(A)

8 Araucária(−25.555481,

−49.4719)

Rural Outdoor Calliphoridaesp.(L)

9 Curitiba(−25.46825,

−49.251617)

Urban Indoor Chrysomyaalbiceps(E)

10 Lapa(−25.627031,

−49.939008)

Rural Outdoor Aleocharapseudochrysorrhoa(A),Oxelytrumdiscicolle(A),

Oxelytrumerythrurum(A),Philonthushepaticus(A)

11 Araucária(−25.582414,

−49.370833)

Rural Outdoor Oxelytrumdiscicolle(A),Oxelytrumerythrurum(A),Peckia

(Pattonella)resona(A)

12 Curitiba(−25.595833,

−49.288333)

Rural Outdoor Hemiluciliasemidiaphana(L),Paraluciliapseudolyrcea(L)

13 Curitiba(−25.521317,

−49.301283)

Urban Outdoor Sarconesiachlorogaster(L)

14 FazendaRioGrande

(−25.63155,−49.110728)

Rural Outdoor Chrysomyaalbiceps(L/A),Cochliomyiamacellaria(A),

Creophilusvariegatus(A),Hemiluciliasemidiaphana(A), Ophyraaenensis(A),Oxelytrumerythrurum(A)

15 QuatroBarras(−25.392161,

−49.032953)

Rural Outdoor Oxelytrumdiscicolle(A),Paraluciliapseudolyrcea(L)

16 Curitiba(−25.50985,

−49.213311)

Rural Outdoor Chrysomyaalbiceps(L),Oxelytrumdiscicolle(A)

17 Curitiba(−25.433272,

−49.276792)

Urban Indoor Microcerellahalli(L/P),Sarconesiachlorogaster(L)

18 CampoMagro(−25.3461,

−49.422619)

Rural Outdoor Hemiluciliasemidiaphana(L),Oxelytrumdiscicolle(A),

Oxelytrumerythrurum(A)

19 Colombo(−25.332906,

−49.149128)

Rural Outdoor Chrysomyaalbiceps(E/L),Hemiluciliasemidiaphana(E/L),

Paraluciliapseudolyrcea(E/L),Peckia(Pattonella)resona (E/L)

20 Araucária(−25.665444,

−49.351297)

Rural Outdoor Euspilotusazureus(A),Oxelytrumdiscicolle(L/A),Philonthus

sp.(A)

21 PontaGrossa(−25.131439,

−50.157911)

Urban Indoor Chrysomyaputoria(E/L/A)

22 CampinaGrandedoSul

(−25.350311,−49.065567)

Rural Outdoor Luciliaeximia(E)

23 Curitiba(−25.601817,

−49.33875)

Rural Outdoor Oxelytrumdiscicolle(L/A)

−49.94755)

Rural Outdoor Chrysomyaalbiceps(L/P/A),Dermestesmaculatus(L),

Euspilotusazureus(A),Oxelytrumdiscicolle(L/A),Piophila casei(L/P)

−50.15275)

Urban Indoor Chrysomyaalbiceps(L),Dermestesmaculatus(L),Phoridae

sp.(L)

throughgreatereffortstowardcollectionandidentiﬁcation(Corrêa etal.,2014).

ThepredatoryfamiliesStaphylinidaeandHisteridaerepresent halfoftheidentiﬁedColeopteraspecies(Table3).Staphylinidae hadthreecollectedspecies,nonewithpreviousrecordsonhuman corpses. Aleochara pseudochrysorrhoais the only with previous recordsinexperiments.AccordingtoMiseetal.(2007),thisspecies isprevalentduringspringandsummer,makingitanimportant sea-sonalindicator.AdultsofA. pseudochrysorrhoapreyonmaggots, andlarvaeareparasitoidsofpupae,leavingthehostasthirdinstar larvaeandpupating inthesoil(Rotheetal.,unpublisheddata). CreophilusvariegatuswasﬁrstrecordedbyLuederwaldt(1911)and istheonlyknownrecordofitsgenusinBrazil(seeAlmeidaetal., 2015).ThelastStaphilinidaespeciesisP.hepaticus,alsoanot pre-viouslyrecordedin eitherexperimentalstudiesor casestudies. Philonthusisconsistentlyreportedbyseveralresearchers(e.g.Mise

etal.,2007;Santosetal.,2014;SouzaandLinhares,1997)who conductedcarrionecologystudies.However,thegreattaxonomic difficultly of classifyingStaphylinidae rarelyallowspecies level identification.TheHisteridaespeciespresentedonthisstudywere previouslyreportedby Miseetal. (2007).AlthoughH.cavifrons waslateridentifiedbyCellietal.(2015),bothspeciesrecordedin thepresentstudywerenotedforthefirsttimeonhumanbodies. Euspilotusazureuswasnotedinexperimentscarriedoutonother Brazilianregions(SouzaandLinhares,1997;Souzaetal.,2008).It isknownthatbothlarvaeandadultsofE.azureuspreyonDiptera eggsandmaggots,andlifecycleanddevelopmentequationsfor thisspecieswerepresentedbyCaneparoetal.(2017).Thereis lit-tleinformationavailableforH.cavifrons,thoughCaterino(1999)

statesthisspeciesshowspreferenceformoisthabitats.

Dipteraprovidesthebulkofentomologicalevidencein most deathinvestigationsandarethemoststudiedgroupinforensic

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Table2

CompletelistofidentiﬁedspeciescollectedatdeathscenesbytheCSIpersonnel.Includingnumberofcaseswitheachspeciesandfamily,andtheproportion(=relative frequency)ofoccurrenceofspeciesandfamilies.

Order Family Species Cases Cases

(family)

Proportion– species(%)

Proportion– family(%)

Coleoptera Dermestidae Dermestesmaculatus 2 3 8 12

Dermestesperuvianus 1 4

Histeridae Euspilotusazureus 2 3 8 12

Histercavifrons 1 4

Hydrophilidae Pelosomaaff.lafetertei 1 1 4 4

Silphidae Oxelytrumdiscicolle 11 12 44 48

Oxelytrumerythrurum 4 16

Staphylinidae Aleocharapseudochrysorrhoa 1 4 4 16

Creophilusvariegatus 1 4

Philonthushepaticus 1 4

Philonthussp. 2 8

Diptera Calliphoridae Chrysomyaalbiceps 10 19 40 76

Chrysomyaputoria 1 4 Cochliomyiamacellaria 1 4 Hemiluciliasemidiaphana 6 24 Luciliaeximia 1 4 Luciliasericata 1 4 Paraluciliapseudolyrcea 5 20 Sarconesiachlorogaster 4 16 sp. 1 4

Muscidae Muscadomestica 1 3 4 12

Ophyraaenensis 2 8

Phoridae sp. 1 1 4 4

Piophilidae Piophilacasei 1 1 4 4

Sarcophagidae Microcerellahalli 1 3 4 12

Peckia(Pattonella)resona 2 8

entomology(e.g.Alvesetal.,2014;Greenberg,1991).Considering availableregionaldata,onlyC.macellariaandP.caseiwerenot pre-viouslynotedintheregion.ParaluciliapseudolyrceaandP.resona werenotedfortheﬁrsttimeonhumanbodies(Table3).

Amongtheﬁvefamiliescollected,Calliphoridaewaspresentin 76%ofthecasesstudied.Eightspecieswererecordedfromthis fam-ily.P.xanthogeineateswastheonlyspeciesnotpreviouslyrecorded onhumanbodies in Brazil(Table 3).Chrysomya albicepsis one ofthemostcommonnecrophagous speciesandwasthesecond mostfrequentspeciespresentamongcases.AlthoughC.albiceps isoneofthemostcitedspeciesinBrazilianforensicentomology cases(Kosmannetal.,2011;Vairoetal.,2015b;Vasconcelosetal., 2014)and experiments(e.g.Carvalhoet al.,2000;Mouraetal., 2005;SouzaandLinhares,1997),there isnopublished biologi-caldatafortheBrazilianC.albicepspopulationusingnaturaldiets (Estradaetal.,2009usedartiﬁcialdiets).Chrysomyaputoriawas col-lectedinoneindoorcase.Itisworthwhiletonotethatwhilesome authorsclaimcarrionisnotthepreferredmediumforoviposition (SouzaandLinhares,1997)forthisspecies,othershaveobserved thisspeciescolonizinghumanbodies(Oliveira-Costaetal.,2001). Cochiliomyiamacellariawasobservedinjustonecase.Itspresence inarurallylocatedcasesupportsByrdandCastner’s(2010) obser-vationthatthisspeciesisrarelyrecoveredfromindoorhabitats. Thisspecies,responsibleforcasesofsecondarycutaneousmyiasis inanimalsandhumans,isalsoofmedicalandveterinary impor-tance(Kolleretal.,2011).Hemiluciliasemidiaphanawasthethird mostfrequentspecies,althoughpreviousrecordsfromcadavers arelimitedtoCarvalhoetal.(2000)(ILMcollection)andVairoetal. (2015b)(Case6).TwospeciesofLuciliawerecollectedintwo sep-aratecases,L.eximiainarurallocationandL.sericatainanindoor urbancase.LuciliaeximiawasreportedbyCarvalhoetal.(2000)and inOliveiraandVasconcelos’s(2010)regionalexperimentsatILM, duringwhichthespecieswascollectedinaforestfragmentarea.

Vairoetal.(2015b)describedtheoccurrenceofL.sericatainan indoorcase(case6).Nodatawasavailablebeforethispublication. Paraluciliapseudolyrceawascollectedonlyinruralareas,aﬁnding alsoreportedbyMouraetal.(2005).Thisstudyistheﬁrstinstance

ofthisspeciesinaforensicentomologycaseinBrazil.Thelast Cal-liphorid,S.chlorogaster,hasbeennotedinpreviousexperiments andismentionedintwopublishedcasestudies(basedoncases 6and17–Table1).Sarconesiachlorogasterisahighlyprevalent speciesinSouthernBrazilandtheavailablebiologicaldata(Lecheta etal.,2015)allowsforitsuseinPMIestimation.

BothspeciesofMuscidaewerecollectedonpreviousﬁeld stud-ies(Mouraetal.,2005;Silveira,2007)andreportedonILMpremises (Oliveira-Costaetal.,2001;OliveiraandVasconcelos,2010).Musca domesticaisacommonspeciesassociatedwithhumandwellings andisusuallynotfoundonfreshcorpses(ByrdandCastner,2010). OneadultspecimenwascollectedonCase1inaruralarea,but thespecimenwasnotusedforPMIestimate.AdultsofO.aenensis werecollectedonruralareasontwocases(Cases7and14).Despite notbeingusedforPMIestimate,bothspecies,M.domesticaandO. aenescens,havepotentialforensicimportanceduetotheir sarcos-aprophagoushabits,andhavebeenmentionedincarrionecology studies(Barbosaetal.,2009).AlthoughMuscidaehasaconsistent presenceincarrionecologystudiesandILMcollections,the poten-tialuseofthefamilyinPMIestimationhasyettobeassessedin Brazil.

PiophilacaseiwastheonlyPiophilidaerecordedinthisstudy, recoveredincase24aslarvalandpupalspecimensonacorpseina rurallocation.Thespecieshasnotbeenreportedinregional stud-ies,althoughPiophilidaesp.wascollectedbyMouraetal.(2005).

Carvalhoetal.(2000)wastheonlyonetocollectthisspeciesinan ILM.LarvaeofP.casei,knownas“cheeseskippers”,areacommon storedproductpestwithcosmopolitandistribution(Smith,1986). Whenpresentondeadbodies,larvaeofthisspeciesareusually associatedwithlaterstagesofdecomposition(ByrdandCastner, 2010).Biologicaldataonthespeciesisavailable(Russoetal.,2006), butwasnotreferencedduetothepresenceofbetterindicatorsand theimpossibilityofspeciesidentiﬁcationatthetime.

Microcerellahalliand Peckia resona werereportedin experi-mentsbyMouraetal.(1997,2005)andVairoetal.(2011).OnlyM. hallihasbeencollectedonaBraziliandeathscene(Vairoetal.,2017

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Table3

Speciescollectedoncasesincomparisonwithpreviousinformationfromregionalstudiesandtheirforensicimportance.

Order Family Species Regionalexperimentaldata Potentialforensicimportance

(Brazil)

Coleoptera Dermestidae Dermestesmaculatus Miseetal.(2007) Carvalhoetal.(2000)b

Dermestesperuvianus Firstrecordc

Histeridae Euspilotusazureus Miseetal.(2007,2013) Firstrecordc

Histercavifrons Miseetal.(2007)(afterCelli etal.,2015)

Firstrecordc

Hydrophilidae Pelosomaaff.lafetertei Firstrecordc

Silphidae Oxelytrumdiscicolle Mouraetal.(1997)andMise etal.(2007)

Firstrecordc

Oxelytrumerythrurum Almeidaetal.(2015) Firstrecordc

Staphylinidae Aleocharapseudochrysorrhoa Corrêaetal.(2014),Miseetal. (2007,2013)

Firstrecordc

Creophilusvariegatus Firstrecordc

Philonthushepaticus Firstrecordc

Diptera Calliphoridae Chrysomyaalbiceps Silveira(2007) Kosmannetal.(2011)a_,_Vairo

etal.(2015b)a_,_Vasconcelos

etal.(2014)a

Chrysomyaputoria Silveira(2007) Oliveira-Costaetal.(2001), Salviano(1996)b_,_Vasconcelos

etal.(2014)a

Cochliomyiamacellaria Carvalhoetal.(2000)b_,

Oliveira-CostaandMello-Patiu (2004)a

Hemiluciliasemidiaphana Mouraetal.(1997,2005), Silveira(2007)

Carvalhoetal.(2000)b_,_Vairo

etal.(2015b)a

Luciliaeximia Mouraetal.(1997,2005), Silveira(2007)

Carvalhoetal.(2000)b_,_Oliveira

andVasconcelos(2010)b

Luciliasericata Mouraetal.(2005) Vairoetal.(2015b)a

Paraluciliapseudolyrcea Mouraetal.(2005),Silveira (2007)

Firstrecordc

Sarconesiachlorogaster Mouraetal.(1997,2005), Silveira(2007)

Vairoetal.(2015b,2017)a

Muscidae Muscadomestica Silveira(2007) Oliveira-Costaetal.(2001)b_,

OliveiraandVasconcelos (2010)b

Ophyraaenensis Mouraetal.(2005),Silveira (2007)

Oliveira-Costaetal.(2001)b

Piophilidae Piophilacasei Carvalhoetal.(2000)b

Sarcophagidae Microcerellahalli Mouraetal.(2005),Vairoetal. (2011)

Vairoetal.(2017)a

Peckia(Pattonella)resona Mouraetal.(1997,2005), Vairoetal.(2011)

Firstrecordc a_Brazilian_case_report.

b_ILM_collection.

c _First_recorded_instance_in_Brazilian_death_scenes.

M.hallilarvaeandpupaewerecollectedfromanindoorurbanscene (Case17),andP.resonaadults(Case11)andeggsandlarvae(Case 19)werecollectedatruralscenes.

Conclusion

Thepresentstudyiscurrentlythebiggestcompendiumofinsect speciesassociatedwithdeathscenesinBrazil.We identified23 species,elevenofwhichhavenotbeenpreviouslynotedonhuman corpses.Despitesubstantialliteratureregardingregionalfauna,we observedfivespeciesthathavenotbeenreportedinearliercarrion studies.Collaboratingwiththescientificpoliceprovideduswitha betterpictureofwhichspecieswerelessunderstoodandguided thefocusofourinvestigation.Duetothereoccurringpresenceof certainspeciesacrossthecases,biologystudiesforS.chlorogaster (Lechetaetal.,2015),E.azureus(Caneparoetal.,2017),O.discicolle andO.erythrurum(Caneparo,2017),A.pseudochrysorrhoa(Rothe etal.,unpublisheddata)andthedescriptionoftheimmaturestages ofParaluciliapseudolyrcea(Silvaetal.,2018)werepublishedorin pre-publication.Producingliteratureonthebiologyofforensically relevantspeciesisanimportantaspectofforensicentomology;as morespeciesbecomerelevanttoforensics,referencesfor biologi-caldataarenecessarytoutilizetheinformationthesespeciescan provideinaninvestigation.

Asanyscience,forensicentomologyneedsbackground informa-tiontobeaspreciseandreliableaspossible.Familiarizingoneself withlocalfaunabeforeinvestigatingadeathsceneisasimpleyet underestimatedprocedure.Forthisreason,westronglyadvisethat forensicentomologygroupsdonotrushintocasestudies.Tothis end,wesuggestconsultingPujol-Luzetal.’s(2008b)directivesfor Brazilianforensicentomology,whichadvisesconductingstudiesin taxonomy,biology,andsuccession.Inadditiontothesemeasures, exhaustivesurveysindifferentregionsofthecountrycanenable investigatorsorscientiststomakemoreaccurateestimationswith greaterspeciﬁcity.Itisourintentionthatthedatapresentedinthis studycanguidenewstudiesinforensicentomologyand encour-agepartnershipbetweenscientiﬁcacademiaandlawenforcement agencies.

Conﬂictsofinterest

Theauthorsdeclarenoconﬂictsofinterest.

Acknowledgements

WewouldliketothankPolíciaCientíﬁcadoParanáandtheir CSIcrewforthecooperation.TheZoologyDepartmentof Universi-dadeFederaldoParaná,LaboratóriodeSistemáticaeBioecologiade

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Coleoptera,LaboratóriodeDinâmicasEcológicaseLaboratóriode Sistemática,andEvoluçãoeBiogeografiadeDipteraandtheirPI.s fortheinfrastructureandsupport.Andthefollowingspecialistsfor theirvaluablehelponspeciesidentification:FernandoLeivasand DanielMoura(Histeridae),AngelicoAsenjo(Staphylinidae), Clau-dioCarvalho(Diptera),SabrinaRochefort(Piophilidae).AlsotoAnn Georgeforthelanguagereviewofthemanuscript.

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,athttps://doi.org/10.1016/j.rbe.2019.05.009.

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