A survey of necrophagous blowflies (Diptera: Oestroidea) in the Amazonas-Negro interfluvial region (Brazilian Amazon)

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

REVISTA

BRASILEIRA

DE

Entomologia

AJournalonInsectDiversityandEvolution

Biology,

Ecology

and

Diversity

A

survey

of

necrophagous

blowﬂies

(Diptera:

Oestroidea)

in

the

Amazonas-Negro

interﬂuvial

region

(Brazilian

Amazon)

Eduardo

Amat

a,b,∗

_,

_Marco

_Antonio

_Tonus

_Marinho

c

_,

_José

_Albertino

_Rafael

a

a_Programa_de_{Pós-Graduac¸}_ão_em_Entomologia,_Coordenac¸_ão_de_Entomologia,_Instituto_Nacional_de_Pesquisas_da_Amazônia,_Manaus,_AM,_Brazil

b_Grupo_de_{Investigación}_Ciencias_Forenses_y_Salud,_Facultad_de_{Investigación}_Judicial,_Forenses_y_Salud,_Tecnológico_de_Antioquia_Institución_{Universitaria,}_Antioquia,_Colombia c_Faculdade_de_Filosoﬁa,_Ciências_e_Letras_de_Ribeirão_Preto,_Universidade_de_São_Paulo,_Ribeirão_Preto,_SP,_Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received8July2015 Accepted13October2015 Availableonline6November2015 AssociateEditor:GustavoGraciolli Keywords: Blowﬂyassemblage Calliphoridae Diversity Forensicentomology Mesembrinellidae

a

b

s

t

r

a

c

t

Thefaunaofblowflies(CalliphoridaeandMesembrinellidae)inthreelocalitiesofprimaryAmazonforest coverageintheAmazonas-Negrointerfluvialregionwasassessed.Atotalof5066blowflieswere col-lected,withChloroproctaidiodeabeingthemostabundantspecies(66.3%).Adifferenceinspeciesrichness betweenthelocalitiesZF2andNovoAirãowasobserved.Comparisonamongsampledsitesrevealedno considerablevariationinfaunacomposition,exceptforthespeciesEumesembrinellabenoisti(Séguy1925) andHemiluciliasp.,whoseoccurrencewasobservedonlyinasinglelocality.Apparently,Amazonrivers arenotefficientgeographicalbarrierstoinfluencethecurrentcompositionofnecrophagousblowfly assemblages.Also,mostoftheblowflyspeciesdidnotshowanoticeablespecificityforanyspecificforest amongtheinterfluvialareasoftheombrophilousforest.Finally,anupdatedchecklistofnecrophagous blowflyspeciesoftheAmazonasstateinBrazilispresented.

Introduction

NecrophagousfliesofthefamilyCalliphoridae(Diptera: Calyp-tratae:Oestroidea)areamongthefirstinsectstodetect,arrive,and colonizeanimalcarcassesinmanydistinctenvironments(Hanski, 1987;Amendtetal.,2004).Inaddition,theyhaveaveryimportant roleinthedecompositionprocess(Keh,1985;Smith,1986;Catts andHaskell,1991;SouzaandLinhares,1997;Oliveira-Costa,2008), andspeciesfromthisfamilyareofmajorimportancetoforensicand medicalissues,inthelatterforbeingcarriersofmany pathologi-calmicroorganisms(Greenberg,1971;Amendtetal.,2004;Sawabe etal.,2011).Mesembrinellidae(Diptera:Calyptratae:Oestroidea),a grouphistoricallytreatedasasubfamilyofCalliphoridae,appearsto haveadifferentbiology.Thereproductivesystemofthefemalesis modified;theyareviviparousandlarvaeseemtohaveparasitoidal preferences.Thebiologyoftheimmaturesis stillpoorly under-stood;adultsarestronglyattractedtodungandcarrion,andclearly all species show preferencestoward inhabitingpristine forests (Guimarães,1977).

Inforensicand legalmatters, knowledgeaboutthe distribu-tionandthetolerancetodifferentecologicalparametersofthese necrophagousspeciesiscrucialtoinferthelocaleinwhichdeath,

∗ Correspondingauthor.

E-mail:ecamat@gmail.com(E.Amat).

oratleastthebeginningofthedecomposition,tookplace,aswell astoestimatethepost-morteminterval(PMI)(Greenberg,1991; Amendtetal.,2004;Oliveira-CostaandMello-Patiu,2004;Rocha etal.,2009).Mostofthis knowledge,however,cannotbeeasily extrapolatedto differentlocalities and thespecies assemblages usuallydependonthedegreeofconservationofaparticular envi-ronment(Zabalaetal.,2014).

Species in these families have different tolerances to envi-ronmentalconditions,beingaffectedbytheproximitytohuman populations(synanthropy)anddisturbancesinprimaryvegetation coverage,moreobservableinspeciesofMesembrinellidae,which are absent in disturbed natural areas and urbanenvironments (Polvony,1971;Espositoetal.,2010).Also,differentblowflyspecies presentdistinctdispersalratesandflightcapabilities,with envi-ronmentalelementsactingasbarrierstosome,butnotall,species (MacleodandDonnelly,1960;Tsudaetal.,2009).IntheAmazonian rainforest, largeriversconstitute one of these barriers, histori-calorcurrent,todispersalindifferentgroupsofwingedanimals, suchasbirds(HayesandSewlal,2004),eventhoughthedynamics ofisolatedpopulationsmaypresentmanyotherhistoricalcauses (Haffer,1997).Dataonflightanddispersalcapacityinblowflies isscarce,butthestudiesconductedsofarindicatethattheycan flyforverylongdistances;varyinginasingleflightbetween100 and700mforLuciliaspeciesandfrom1250to1789m—andasfar as3500m/day—forCalliphoranigribasis(Tsudaetal.,2009). More-over,riversaswideas182.88mandslopesashighas152.40mdo http://dx.doi.org/10.1016/j.rbe.2015.10.002

0085-5626/© 2015 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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alreadyimplicatedashistoricalbarriersfordispersalandaccount forthedifferentdistributionofsomebird speciesintheregion (Haffer,1997;HayesandSewlal,2004).Forflies,itcouldalsobe animportantbarrier,sinceinitswiderportionstherivercanbe morethan40kmwideduringtherainyseason.Inthiscontext,this studysurveyedtheblowflyfaunaintheinterfluvialregionofthe Amazonas-Negrorivers,withacomparisonbetweenthespecies richnessandabundanceofthenecrophagousflyfaunainthe sam-pledlocalities.

Materialandmethods

Van Sommeren-Rydon traps, modified to collect flies, were mounted in three localities of the interfluvial region of the Amazonas-Negrorivers betweenDecember 1st and 15th, 2013 (Fig. 1). All localities comprised regions of typical Amazonian rainforestphytophysiognomy witha denseombrophilous forest according to the classification of IBGE (2012). Sampled locali-tiesincluded:(1)theZF2biologicalreserve,located50kmfrom the major urban center in the Manaus municipality; and pri-vate propertiesin the municipalitiesof (2) NovoAirão and (3) CareiroCastanho.Ineachlocality,4–7trapswereused,baitedwith amixtureof decomposingcow,chicken, andfishviscera.Traps wereemptiedafter2–3daysandallfliescollectedwerecounted andidentifiedfollowingthekeysprovidedbyAmatetal.(2008),

Kosmannetal.(2013),Whitworth(2014),andWolffetal.(2014). Datafromthedifferentlocalitieswereanalyzedforrelativeand totalabundancedistributionusingtheIBM-SPSSStatistics(2012)

software.Samplingefficiencyand representation wereassessed usingcurvesforspeciesaccumulation,incidence-basedcoverage estimator(ICE),andtheJack1andtheChao1non-parametric esti-matorsoftotalspeciesrichness,usingtheEstimates9.0.1software (Colwell,2013).Non-parametricKruskal–Wallistestsandpaired Mann–Whitney’sUtestswereusedinordertoevaluateifthere weresignificantdifferencesinrichnessandabundancebetween thelocalities.TheJaccardcoefficientandcomplementarityindex wascalculatedasameasureoftheturnoverandcomplementarity indexinspeciescompositionbetweenlocalities(Colwell,2013).

Results

A total of6772 dipteranswere collected, withCalliphoridae beingthemostabundant(4356specimens—64.3%),followedbythe families Muscidae(715—10.5%),Mesembrinellidae (710—10.4%), Sarcophagidae (325—4.7%), and Fanniidae (203—2.9%). Other Dipterafamilies comprised 463individuals (6.8%). Of the5066 blowﬂy specimens (Calliphoridae and Mesembrinellidae) col-lected, 10 were species of Calliphoridae: Chloroprocta idiodea (Robineau-Desvoidy, 1830), Chrysomya albiceps (Wiedemann, 1819),Chrysomyamegacephala(Fabricius,1794),Chrysomya puto-ria(Wiedemann,1818),Cochliomyiamacellaria(Fabricius,1775), Hemiluciliasegmentaria(Fabricius,1805),Hemiluciliasemidiaphana (Rondani,1850),Hemilucilia sp.and Luciliaeximia(Wiedemann, 1819), and Paralucilia paraensis (Mello, 1969); and 3 were of Mesembrinellidae:Eumesembrinellabenoisti(Séguy,1925), Eume-sembrinellaranda(Walker, 1849), andMesembrinellabellardiana (Aldrich,1922). Boththerarefactioncurve(Fig.2)and the val-uesofthespeciesrichnessestimators,ICE,Chao1,andJack1(96%) (Table 1), indicated that collecting sitesand the complete area assessedwerewellsampled.

Hemiluciliasp.,aspeciesfoundexclusivelyintheZF2locality,is probablyanewspeciessincethemalegenitaliadoesnotmatchany ofthedescribedspeciesofthisgenus(sensuDear,1985–datanot shown).Excludingthisspecies,sampledfaunacomprised12out ofthe18species(66.6%)currentlyknownfortheBrazilian Ama-zonasstate(Table2).Among these,themostabundantspecies wasC.idiodea(66.3%),followedbyE.randa(8.4%)andH. semidi-aphana(5%),whileC.macellariaandC.megacephalaweretheleast abundant,representedbylessthan25individualseach(<0.36%) (Fig.3).WiththeexceptionoftheexclusiveoccurrenceofE.benoisti inNovoAirãoandHemiluciliasp.intheZF2Reserve(Manaus),as wellastheabsenceofC.megacephalainthelatter,allspecieswere foundinthethreelocalitieswithsomewhatdifferentabundances (Fig.4).ComparisonsbetweenlocalitiesshowedthatNovoAirão isslightlyricherthantheothertwo,presenting12outofthe13 sampledspecies,afactalsoobservedintherarefactioncurvefor alllocalities(Fig.2).Non-parametricaltestsshowednostatistically

Novo airão

Collection site Populated place river

ZF2

Rio Negro rive

r Amazon river Amazon rive r Careiro Kilometers Amazon river Manaus 20 0 59°48´W 60°12´W 60°36´W 61°00´W 2°51 ´S 3°15 ´S 3°39 ´S N N

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Cumulative number of specie s 1 2 3 4 5 6 7 8 9 10 11 12 13 0 1 201 401 601 801 1001 1201 1401 1601 1801 2001 2201 2401 2601 ... Careiro – – – NovaAiro

Cumulative number of individuals ZF2

Fig.2.Rarefactioncurvefornecrophagousblowﬂiesinthethreeinterﬂuvialcollectingsites.

Table1

Speciesrichnessestimatorsforeachsiteandforthecompleteareaofstudy.Nt,numberoftraps;Ns,numberofspecies;Ni,numberofindividuals.ICE,incidence-based coverageestimator;Chao1andJack1,1storderChaoandJackniferespectively.%,percentageofthetotalexpectednumberofspecies.

Site Nt Ns Ni ICE Chao1 Jack1 Mean±SD %

CareiroCastanho 4 11 550 11.43 11 11.75 11.4±0.4 96.5

NovoAirão 6 12 1031 12.41 12 12.83 12.4±0.4 96.7

ZF2 7 11 3479 11.43 11 11.86 11.4±0.4 96.2

Completearea 17 13 5060 13.32 13 13.94 13.4±0.5 96.9

significantdifferencesinspeciesabundance(Kruskal–Wallis;df=2, p=0.649);nevertheless,astatisticallysignificantdifferencein rich-nesswasfound(Kruskal–Wallis;df=2,p=0.047).Aposthocpaired testusingMann–Whitneytestsshowedsignificantdifferencesonly

betweenthelocalitiesofNovoAirãoandZF2(p<0.05,r=0.030). Althoughthesestatisticaldifferenceswerefound,highvaluesof theJaccardsimilaritycoefﬁcientandlowvaluesof complementar-itywererecordedinalllocalities.Comparisonsgivenas(Jaccard

4000 3000 2000 1500 1000 Nº of specimens 3500 2500 500 0 C. Idiode a E. rand a H. semidiaphanaHemilucilia spM. bellardian a L. e ximia C. puto ria P. paraensi s E. benoistiC. albicep s H. segmentar ia C. megacephal a C. macellar ia

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Calliphoridae

Chrysomyiinae

Chloroproctaidiodea

(Robineau-Desvoidy 1830)

All Ca,Co,Mao,NvA, RFAD,Urucu Cow,pig,ﬁshand

chickenviscera

Paraluppi(1996),Espositoetal.(2010), Ururahy-Rodriguesetal.(2013) Chrysomyaalbiceps

(Wiedemann1819)

All Ca,Co,Mao,NvA, RFAD,Urucu Cow,pig,ﬁshand chickenviscera

Paraluppi(1996),Barros-Souzaetal. (2012),Espositoetal.(2010), Ururahy-Rodriguesetal.(2013) Chrysomya megacephala(Fabricius 1794) Careiro,Novo Airão

Ca,Co,Mao,NvA, RFAD,Urucu Cow,pig,ﬁshand chickenviscera

ParaluppiandCastellón(1993), Paraluppi(1996),Espositoetal.(2010), Barros-Souzaetal.(2012)

Chrysomyaputoria (Wiedemann1818)

All Ca,Co,Mao,NvA, Manauscity, Urucu

Cow,pig,ﬁshand chickenviscera

ParaluppiandCastellón(1993), Paraluppi(1996)

Cochliomyiamacellaria (Fabricius1775)

ParaluppiandCastellón(1993), Paraluppi(1996),Espositoetal.(2010), Ururahy-Rodriguesetal.(2013) Hemiluciliasegmentaria

(Fabricius1805)

Paraluppi(1996),Espositoetal.(2010), Barros-Souzaetal.(2012),

Ururahy-Rodriguesetal.(2013) Hemilucilia

semidiaphana(Rondani 1850)

Paraluppi(1996),Espositoetal.(2010), Ururahy-Rodriguesetal.(2013) Hemiluciliasouzalopesi

(Mello1972)

– Mao Manauscity Pig Ururahy-Rodriguesetal.(2013)

Hemiluciliasp. ZF2 Mao ZF2 Fishandchicken

viscera

Thisstudy Paraluciliaparaensis

(Mello1969)

All Mao,Co Manauscity,

Urucu

Espositoetal.(2010),Barros-Souza etal.(2012)

Paraluciliasp. – Mao RFAD Pig Ururahy-Rodriguesetal.(2013)

Luciliinae Luciliaalbofusca (Whitworth2014)

– Mao RFAD Flighttrap Whitworth(2014)

Luciliaeximia (Wiedemann1819)

All Ca,Co,Mao,NvA, Manauscity, RFAD,Urucu

Paraluppi(1996),Espositoetal.(2010), Barros-Souzaetal.(2012),

Ururahy-Rodriguesetal.(2013)

Mesembrinellidae

Eumesembrinellabenoisti (Séguy,1925)

NovoAirão Ca,Mao,NvA, RFAD Pig,ﬁshandchicken viscera

Ururahy-Rodriguesetal.(2013) Eumesembrinella

quadrilineata(Fabricius 1805)

– Co Urucu Cowviscera Espositoetal.(2010)

Eumesembrinellaranda (Walker1849)

All Ca,Co,Mao,NvA, Urucu Cow,ﬁshandchicken viscera

Espositoetal.(2010) Mesembrinellabatesi

(Aldrich1922)

Mesembrinella bellardiana(Aldrich 1922)

All Ca,Co,Mao,NvA, Urucu Cow,ﬁshandchicken viscera

Espositoetal.(2010)

Mesembrinellabicolor (Fabricius1805)

coefficient;Complementarityindex)areZF2-NovoAirão:(0.769; 0.23);Careiro-ZF2:(0.833;0.166);andNovoAirão-Careiro(0.916; 0.083).TheestimatedC-scoreforco-occurrence(0.03845)being significantlysmallerthanthecriticalsimulatedindex (0.04157) indicatesthatnecrophagousblowflyspeciesarerandomlyspatially distributed.Thisiscoherentwiththecompositionanddistribution onmostofthespeciesassemblage.

Discussion

Diversitypatternsoftheblowﬂyassemblageareconsistentwith thetrendsfoundinpreviousstudiesfortheAmazonregion(Amat, 2010;Espositoetal.,2010).Thenumberofspeciesreportedhere waslowerthanthatreportedbyEspositoetal.(2010)duringa collectionofthreemonthsinanundisturbedAmazonarea.Our studyalsocorroboratesthedominanceofC.idiodea,E.randa,and

H.semidiaphanaintheAmazoniannecrophagousblowﬂy assem-blages;theseﬁndingsareinagreementwiththoseofEspositoetal. (2010).Thefaunisticcompositionwasalmostthesameexceptfor threespeciesofMesembrinellidaenotfoundinthisstudy: Eume-sembrinella quadrilineata (Fabricius, 1805), Mesembrinella batesi (Aldrich,1922),andMesembrinellabicolor(Fabricius,1805).

The composition and the signiﬁcant difference in richness betweenthelocalitiesofNovoAirãoandZF2maybeexplained astheprobableeffectofthecloserproximitytourbancenters,as shownbytheabsenceinZF2ofC.megacephalainthesampling, anintroducedspecies withhighdispersioncapacityand highly synanthropichabit(PradoandGuimarães,1982;Baumgartnerand Greenberg,1985;ParaluppiandCastellón,1993;Paraluppi,1996), andfortheexclusivepresenceofE.benoistiandHemiluciliasp.in eachofthesetwolocations,respectively.Unfortunatelynodetailed biologicaldataareavailable aboutthesetwo speciestosuggest

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100% 90% 80% 70% 60% 50% 40% 30% 20% 10% Relativ e ab undance

ZF2 Novo Airao Careiro

C. idiodea C. albiceps C. megacephala

C. putoria C. macellaria

E. benoisti E. randa

H. segmentariaH. semidiaphanaHemilucilia. sp L. eximia

M. bellardianaP. paraensis

0%

Fig.4. Relativeabundanceofnecrophagousblowﬂiesineachofthethreeinterﬂuvialcollectingsites.

preliminary inferences about this spatial distribution pattern, althoughsomerarespeciesfromthegenusHemiluciliaandallof Mesembrinellidae used tobe highly asynanthropic(Guimarães, 1977;BaumgartnerandGreenberg,1985).

Accordingtothe values ofthe similaritycoefficient andthe complementarityindices,thethreelocalitiesaresimilarinspecies composition(10speciesshared).Thesefindingsmayindicatethat Amazonriverarenotefficientbarriersforallspeciesassemblage dispersion,atleastinahistoricalperspective.Thethreelocalities sampledarerelativelysimilarintermsofforestphysiognomy;the differencesfoundinthiscontextdonotseemtobeasignificant factorinfluencingthisfaunalassemblageexceptforafewspecies withpossiblegeographicalrestrictedrangesorintrinsicbiological factorsmentionedinthelastparagraph.

Asimilarlevelinabundanceamonginterfluvialsitesandthe randomly spatially distribution jointly with the long dispersal capability of blowflies (Tsudaet al., 2009) allowus to suggest that this interfluvial region acts as a unique area of blowfly populationsinteractions.Differencesinabundancemaybemore noticeable ateven largerareas thanthose studiedhere(mean: 11kmbetweenlocalities)andmoreevidentinhighlyfragmented landscapes (Zabala et al., 2014). The remarkably low densities and abundance for the native species C. macellaria—which is considereda highlysynanthropic species in thePeruvian Ama-zon (Baumgartner and Greenberg, 1985)—maybe explained as a consequenceof therelatively lowhumanimpact onthe sur-veyedareasormayreflect theeffectsofecologicalcompetition with the introduction of the Chrysomya species to the Ameri-cas,sinceC.macellariawasoneofthemostfrequentspeciesand themost abundantflyin thePeruvianrainforest from1979to 1981 (Baumgartner and Greenberg, 1985). It is noteworthy to mentiontheimportanceofassessingtheeffectsoftheseinvasive speciesonthenativecarrionflycommunitiesintheAmazonian region.

Althoughthereseemstobenoevidencesupportingtherivers ashistoricalbarriersaffectingnecrophagousdipteranassemblages distribution in this region, it is still possible that these rivers mayconstitutecurrentbarrierstogene flow,leadingto signifi-cantdifferences inpopulations among interfluviallocalities. An assessmentofpopulationstructureanddifferentiationbasedon molecular data is being conducted and should provide further insightsonthismatterandalsointheforensiccontext.Spatial dis-tributionsofblowfliesarestronglyaffectedbysynanthropiceffects, dispersalcapability,andthelocalandspecializedbreedingsitesof theimmaturestages(Norris,1965;Polvony,1971).Theseaspects mustbetakenintoconsiderationinbiogeographicalinferencesand probablyaccountforalargeextentofthepatternsfoundinthis studyfortheAmazonianforest.

Thechecklistprovidedheremayserveasabaselineforfuture ecological studies and applications in the forensic entomology framework oftheAmazonregion,since alocalfauna inventory is essential in this context. Since a comprehensivestudy must includeabroadtemporaldimensionandconsiderseasonal varia-tionsandtemporalactivitiesofflies,whichvaryduetointrinsic factors (suchas life history, populationdynamics, reproductive cyclesetc.)andextrinsicfactors(temperature,humidity,resources availabilityetc.)(HwangandTurner,2005),thediversitypatterns ofthenecrophagousblowflyassemblagefoundheremustbe inter-pretedwithcautionduetotheshorttimeoffieldcollection.Inthis sensetheyareprobablyunderestimatedcomparedtoalongterm study.Thesefindingsindicatethelackofmonitoringandintensive collectingeffortsandalsothelittleknowledgecurrentlyavailable aboutthecarrionfeedinginsectfaunaofoneoftheworld’smajor megadiversityhot-spots.

Conﬂictsofinterest

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tifying,and countingflies, and toFranciscoXavierFilho forthe valuablehelpwithtrapsandfieldwork.ToDr.NiroHiguchi and JoaquimdosSantos,forpermittingtheuseoftheINPASilviculture Station,atZF2;ToFundaçãodeAmparoàPesquisadoEstadodo Amazonas(FAPEAM)togetherConselhoNacionalde Desenvolvi-mentoCientíficoeTecnológico(CNPq)bythefinancialsupportto theProjectPRONEX,Edital016/2006,Proc.1437/2007.CNPq (Pro-cess472237/2009-8)providedfinancialsupport.JARisfinancially supportedbytheConselhoNacionaldeDesenvolvimentoCientífico eTecnológico(CNPq)(grant300305/2007-9)andMATMwas sup-portedbyFundaçãodeAmparoàPesquisadoEstadodeSãoPaulo (FAPESP-2012/23200-2).

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