Diurnal flight periodicity of a Neotropical ant assemblage (Hymenoptera, Formicidae) in the Atlantic Forest

REVISTA

BRASILEIRA

DE

Entomologia

Biology,

Ecology

and

Diversity

Diurnal

flight

periodicity

of

a

Neotropical

ant

assemblage

(Hymenoptera,

Formicidae)

in

the

Atlantic

Forest

Rodrigo

M.

Feitosa

_,

_Rogério

_R.

_da

_Silva

_,

_Alexandre

_P.

_Aguiar

a_{UniversidadeFederaldoParaná,DepartamentodeZoologia,Curitiba,PR,Brazil}

b_{MuseuParaenseEmílioGoeldi,Coordenac¸ãodeCiênciasdaTerraeEcologia,Belém,PA,Brazil}

c_{UniversidadeFederaldoEspíritoSanto,DepartamentodeCiênciasBiológicas,Vitória,ES,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received17March2016

Accepted31May2016

Availableonline24June2016

AssociateEditor:EduardoA.B.Almeida

Keywords: Malaise Phenology Reproduction Summertime Swarm

a

b

s

t

r

a

c

t

Inthisstudywedocumentforthefirsttimeflightpatternsalonga24htimerangeforanantassemblage inoneofthemostdiverseecosystemsonEarth,theBrazilianAtlanticForest.Malaisetrapswereusedto analyzethediurnalnuptialflightsofaNeotropicalantassemblageduringfivedays.Trapscaptured802 individuals,revealingaremarkablyhighdiversity(42antspecies),withsamplesstronglymalebiased (1:22).Contrariwisetosimilarstudies,wefoundonlyasmallproportionofspeciesengagedinnocturnal nuptialflights,withdiurnalflightsaccountingforanimpressive95%ofallantflightactivityrecorded.For the18mostcommonspecies,threeantgroupscouldbeidentifiedregardingflightperiod:sunrise,sunset, andcontinuousflightactivity.Similarityanalyses,however,suggestthatcloselyrelatedtimerangesof flightactivitymayactuallynotbecontinuous.Further,threespeciesshowedpulsedflightactivity,at variedhoursoftheday.TwospeciesofHypoponerashowedflightactivityatdifferentperiodsoftheday, suggestingcongenericstaggerednuptialflights.Ourresultsmatchlong-termstudiesofantassemblages showinghighdiversityofflightphenologiesinhyperdiversetropicalantassemblagesandprovidethe firstdataonthereproductivephenologyforseveralNeotropicalantspecies.

©2016SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Despitethefactthatantsareabundantand dominant mem-bersofalmosteveryterrestrialecosystem(WilsonandHölldobler, 2005),surprisinglylittleisknownabouttheirreproductiveecology, apparentlyamountingtotheworksofKasparietal.(2001a,b),Dunn

etal.(2007),Nascimentoetal.(2011),Shiketal.(2012),andHelms

andKaspari(2014).Herein,weinvestigatethetimingof

reproduc-tion,a keycomponentofreproductiveecology.Itinfluencesthe timingofsubsequentlifestages, thepotentialforhybridization, theformsofreproductionthatarepossible,andevenpotentially theabilityofaspeciestocoexistinlocalassemblages(Kasparietal.,

2001a;Dunnetal.,2007).

Duetoitsimportance,reproductivebehaviorispreciseand con-stantinmostantspecies(Andersen,1991).Withsomeexceptions, malesandfemaleshavetorelyonmeetingeachotherformating throughnuptialflights(Noordijketal.,2008).Antcoloniesmust synchronizeflightssoastooptimallyoutbreed,findanest,and

∗ Correspondingauthor.

E-mail:[email protected](R.M.Feitosa).

beginthefledglingcolony’sgrowthphase(Kasparietal.,2001b). Inotherwords,nuptialflightsreflectanantcolony’sinvestment in sexualreproductionand dispersal.Yet, littleis knownabout community-widepatternsofalates’phenology(e.g.,seecomments

inTschinkel(1991),andtheshortlistofreferencesinNascimento

etal.(2011)).

Mostdataonantnuptialflightsrefertospeciesfromtemperate zones(BoomsmaandLeusink,1981;Dunnetal.,2007;Noordijk

etal.,2008;Woyciechowski,1987,1992),andaconsiderable

pro-portionoftheinformationisbasedontheobservationofasingle flightorjustafewswarmevents(e.g.,Eberhard,1978;Conway,

1996;Buschinger,2003).Thefewlong-termstudiesavailableon

theflightphenologyoftropicalantsdealpredominantlywith sea-sonalpatterns(Kasparietal.,2001a,b).Theexceptionisthework

ofTorresetal.(2001),whichpresentsthenocturnalperiodicitiesof

antnuptialflightsinthetropicalislandofPuertoRico,usinglight trapsinspectedregularlythroughouttheyear.

Preciseinformationabouttheperiodicityofantnuptialflights througha24htimescaleislargelyunavailable,andlimitedtoa

fewtaxa(Kannowski,1959,1969;Hölldobler,1976).Ouraimwas

todescribethetaxonomicandtemporalpatternsofnuptialflights ofanantassemblageinthetropicsthroughafull24htimescale. http://dx.doi.org/10.1016/j.rbe.2016.05.006

0085-5626/©2016SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://

Materialandmethods

Thisstudy wasperformedin the BoracéiaBiologicalStation (BBS),a96haareawithina16,450hawatershedreserveofAtlantic rainforest,situatedinthestateofSãoPaulo,southeasternBrazil (23◦38S, 45◦53W).TheBBSisinsertedintheTropicalAtlantic morphoclimaticdomain,900mabovesealevel.Descriptionsofthe localvegetationcanbefoundinWilms etal. (1996).The aver-ageannualrainfallbetween1973and1994was2024mm,andthe meantemperatureforthesameperiodwas17.9◦C(DAEE,1994).

SpecimenswerecollectedduringfivedayswitheightMalaise traps(Townes,1972),withtwogroupsoftwotrapsdistributedin eachofthetwomaintrailsintheBBS(TrilhadosPilõesandTrilha doDivisor).Ineachgroup,thetwotrapsweresetatapproximately 100monefromanother.Thegroupsoftwotrapsineachareawere setatapproximately200mfromeachother,andbothgroupsoffour trapswereapproximatelyat1.5kmfromeachother.Alltrapswere setalongday1(21February2005),andthensynchronously emp-tiedatday2,at06:00h(DST).Eachtrapwascheckedexclusivelyby oneperson.Thetrapswerethencheckedeveryfullhour,starting at07:00hofday2.Ateverychecking,thesamplesofeachgroupof twotrapswerecombinedintoonesample;thiswasdoneinorder togeneratemorerobustsamplesof1hintervals.Acompleteround of24hofsamplingwasachievedfromthe06:00–07:00hsample ofday2tothe05:00–06:00hsampleofday3,thereforegenerating 24samplesforeachpoint(twoMalaises),or96samplestotal(two pointsineachofthetwotrails).Theprocessofhourlysamplingwas repeatedanotherfourtimesfortheperiodcomprehendedbetween 06:00and18:00hofdays3,4,5,and6,foralltraps,thus generat-inganother192samples(48samples/day×4days).Thetrapswere notcheckedfrom18:00hintheeveningto06:00hinthemorning betweendays4and7;thematerialcollectedduringthisperiod,for eachnight,wasconsolidatedintoasinglesampleforeachMalaise trappair,thereforegenerating4moresampleseachnight,or16 samples.Duetologisticproblems,the48samplesofonediurnal period(day3)werepooledandthedataexcludedfromthe anal-yses,beingusedonlyasreferencematerialfortheidentifications. Overall,256sampleswereusedfortheanalyses.

AllantspecimenswerepinnedanddepositedintheMuseude ZoologiadaUniversidadedeSãoPaulo(MZSP)antcollection. Mate-rial processing followed the procedures listed in Kaspari et al.

(2001a,b).Antswereidentifiedbytheauthorstospeciesand

mor-phospeciesthroughtheliteratureandbycomparingthespecimens withdeterminedmaterialattheMZSP.Femalesofallspecieswere identifiedtogenus,butourabilitytoidentifyalatestospeciesvaried acrosstaxa.Keysareavailableforalatesofonlyafewgenera,and identifiedseriesinmuseumsoftenlackassociatedalates.Malesof antsareevenmoredifficulttosorttospecies,becauseoftheirhighly conservativemorphology(YoshimuraandFisher,2011).Theywere thensortedtogenus,whenpossible,andtospecies/morphospecies, inallcasesrelyingheavilyonmatchingspecimensattheMZSP collection.

Ant flight activity at BBS was evaluated according to 13 timegroups yieldedbytheexperimentaldesign:12 diurnal1h periods(from06:00–07:00hto17:00–18:00h)andoneperiodof nocturnalflights(18:00–06:00h).Variationin dailyflight activ-itywasevaluatedgraphically,plotting therelationshipbetween hourand number ofindividuals captured givensubfamily, day, Malaisetraporthemostfrequentantspecies.Wedescribethese relationships fitting a nonparametric regression using a loess smoother (loess function in R; R Core Team, 2015). The diel flight activity of the local ant assemblage was further exam-ined using cluster analysis based on unweighted arithmetic averageas linkagemethodand Jaccard(binary)similarity mea-sure,butresultswithSorensen(quantitative)andBaroni-Urbani Buser(binary)coefficientsproducedidenticaltreetopology.The

clusteranalysiscombinedwithJackknifeproceduretoevaluatethe stabilityofthedendrogramtopology(Table2)wasperformedat

www2.biology.ualberta.ca/jbrzusto/cluster.php.

Results

Field work produced 256 useful samples, equivalent to 32 Malaise-trapdays(originaldataavailableassupplementary mate-rial).Atotalof802individualalatesfrom42antspeciesand18 generawerecollected.Malaisetrapsamplingwasstronglymale biased,withonly36femalescaptured,nearly1:22.Alatecatches persamplevariedfromjustoneindividual(18:00–06:00h)upto 139individuals(14:00–15:00h).Only46individuals(5.7%)were

Table1

AbundanceofalatescapturedatReservaBiológicadeBoracéiaalong24hoftheday,

duringaperiodof5days.

Taxa Males Queens Total

alates

Amblyoponinae 15 – 15

Stigmatommaarmigerum(Mayr,1887) 13 – 13

StigmatommaelongatumSantschi,1912 2 – 2

Dorylinae 11 – 11

Cerapachyssp. 11 – 11

Ectatomminae 5 – 5

Gnamptogenyssp. 5 – 5

Formicinae 83 3 86

AcropygagoeldiiForel,1893 83 3 86

Heteroponerinae 4 2 6

Heteroponeradolo(Roger,1860) – 2 2

Heteroponerasp. 4 – 4

Myrmicinae 290 10 300

AcanthognathusrudisBrown&Kempf,1969 13 – 13

Acanthognathussp. 23 – 23

Crematogastersp. 2 – 2

Hylomyrmareitteri(Mayr,1887) 85 1 86

Octostrumarugifera(Mayr,1887) 16 – 16

Pheidolesp.1 – 2 2 Pheidolesp.2 – 1 1 Pheidolesp.3 – 1 1 Pheidolesp.4 22 – 22 Pheidolesp.5 13 – 13 Procryptocerussp. 1 – 1 Rogeriasp. 67 – 67 Solenopsissp.1 11 2 13 Solenopsissp.2 11 1 12

StrumigenyssaliensMayr,1887 12 2 14

Strumigenyssp.1 3 – 3 Strumigenyssp.2 1 – 1 Strumigenyssp.3 1 – 1 Strumigenyssp.4 7 – 7 Strumigenyssp.5 1 – 1 Myrmicinaesp. 1 – 1 Ponerinae 358 21 379

AnochetusaltisquamisMayr,1887 1 – 1

Hypoponeradistinguenda(Emery,1890) 47 11 58

Hypoponeraiheringi(Forel,1908) – 3 3

Hypoponeratrigona(Mayr,1887) 106 2 108

Hypoponerasp.1 80 – 80 Hypoponerasp.2 – 2 2 Hypoponerasp.3 3 – 3 Hypoponerasp.5 86 1 87 Hypoponerasp.6 6 2 8 Pachycondylasp.1 16 – 16 Pachycondylasp.2 5 – 5 Pachycondylasp.3 3 – 3 Pachycondylasp.4 3 – 3 Ponerinaesp. 2 – 2 Total 766 36 802

35 Malaise 1 Malaise 2 Malaise 3 Malaise 4 Number of individuals 30 25 20 15 10 5 0 06-07 07-08 08-09 09-10 10-1111-12 12-13 Hours 13-14 14-15 15-16 16-17 17-18

Fig.1.TherelationshipbetweenhourandflightactivityofaNeotropicalant assem-blagegivensamplingeffort(fourMalaisetraps),basedonhourlysamplingsummary fromfivedays.Thesolidlineswereobtainedbythelocallyweightedsmoother (functionloessinR).

presentinthenocturnalsamples.Eightspecieswererepresented byasingleindividualandsixbytwoindividuals(Table1).

MalaisetrapssampledmainlythesubfamiliesPonerinae and Myrmicinae,which accountedfor 47.3% and 37.4% of the indi-viduals,respectively.Formicinaecomprised10.7%ofthecatches. SimilarlylowvalueswerefoundforAmblyoponinae(1.6%), Doryli-nae(1.4%),Heteroponerinae(0.7%)andEctatomminae(0.6%).

ThemonitoredMalaisetrapsshowedstrongvariation inthe totalnumberofdailyflights(Fig.1).Mostindividualswererecorded between10:00and 15:00h. Bothindividualtraptotalsandthe combinedtotalnumberofindividualscapturedduringthefivedays ofobservation(dailytotal) suggestthat flightactivityincreases fromdawnuptountil15:00h,andthenabruptlydeclinestoward 18:00h(Fig.1).Thisisalsosomewhatevidentonadaybyday analy-sis(Fig.2),andagainfortheFormicinaeandMyrmicinaeseparately (Fig.3).Forothersubfamilies,flightactivitymightappeartobe continuousthroughouttheday,buttherearetoofewspecimensto allowforreliableconclusions(Fig.3).

40 Day-1 Day-2 Day-3 Day-4 Day-5 30 20 Number of individuals10 0 06-07 07-08 08-09 09-10 10-11 11-12 12-13 Hours 13-14 14-15 15-16 16-17 17-18

Fig.2.TherelationshipbetweenhourandflightactivityofaNeotropicalant

assem-blagethrougha24htimescale.Thesolidlineswereobtainedbythelocallyweighted

smoother(functionloessinR).

35 Amblyoponinae Heteroponerinae Dorylinae Myrmicinae Ponerinae Ectatomminae Formicinae Number of individuals 30 25 20 15 10 5 0 06-07 07-08 08-09 09-10 10-11 11-12 12-13 Hours 13-14 14-15 15-16 16-17 17-18

Fig.3.Therelationshipbetweenhourandflightactivityofantsubfamiliesfrom

aNeotropicalassemblagecapturedthrougha24htimescale.Thesolidlineswere

obtainedbythelocallyweightedsmoother(functionloessinR).

Eighteenspecieswitheightormoresampledindividualsmade up92%ofthecombinedtrapcatch(738individuals).Flight activ-ityhoursalongthe5daysvariedmuch(Fig.4a–c),occupyingall timezones,inadistinctstratificationpattern(Fig.5).Visually,three quantitativeclustersseemapparentinFig.5:threespeciesinthe 6–9hrange(topleft),elevenspeciesconcentratingwithin10–15h, andthenfivespeciesmostfrequentlyobservedafter16h. Similar-ityanalyses(Table2),onitsturn,arequiteconsistentinsuggesting threefunctionalgroupsofflightactivity:(1)7–9hand16–18h,(2) 9–12hand15–16h,and(3)12–15h.

All Hypoponera species (Ponerinae) and Hylomyrma reitteri

(Figs.4aand5),aswellas,toacertainextent,Rogeriasp.

(Myr-micinae)andCerapachyssp.(Dorylinae)(Figs.4cand5)seemtofly continuouslyalongtheday,althoughHypoponeradistinguendawas moreactiveinthefirsthoursoftheday(06:00–09:00h).Rogeria

sp.(Figs.4cand 5)showedawiderangeofdiurnal flight

activ-ity,andaunimodalcurve.Ingeneral,malesofcommonspecies showeddistinctandhighlypulsedflightactivity.Acropygagoeldii (Formicinae)andPheidolesp.1(Myrmicinae)hadarestrictperiod offlightwithastrongpulseat13:00–15:00h(Fig.4b),while Pachy-condylasp.1(Ponerinae)presentedastrongpulseat06:00–07:00h (Fig.4b).Trap-jawspeciesinthegeneraAcanthognathusand Stru-migenys(Myrmicinae)seemtoflyintheafternoon,between14:00 and 18:00h(Fig.4c). Species knowntopossess thicker integu-ment,Pheidolespp.,Solenopsisspp.,Stigmatommaarmigerum,and Octostruma rugifera, flew at the hottest hours of the day.It is interestingthatthetwocommonestspeciesofHypoponerahave differentnuptialflightpeaks,withH.distinguendaflyingearlyin themorningandH.trigonaatsunset.

Discussion

Our data represent a first trial to describe in detail the flight phenology ofa tropicalantassemblage. Dailyand hourly samplingdesignforstudyingantphenologyisacomplexand time-consumingtask,stretchedbythelackoftaxonomicinformation regarding alateants. Consideringtherelativelyshortexposition periodoftheMalaisetraps,onenotablefindingofthisstudyisthe significantnumberofantspeciescollected(42speciesin18 gen-era).Thisfactiscertainlyrelatedtotheveryhighdiversityofthe

14 15 10 5 0 12 10 8 6 4 2 0 2.0 1.5 1.0 0.5 0.0 8 6 4 2 0 8 6 4 2 0 3.0 2.5 2.0 1.5 1.0 0.5 0.0

12 Hylomyrma reitteri Hypoponera distinguenda

Hypoponera trigona Hypoponera sp.5

Hypoponera sp.6 Pheidole sp.1 Acanthognathus rudis Solenopsis sp.1 Hypoponera sp.1 Pachycondyla sp.1 Acanthognathus sp. Acropyga goeldii 10 8 6 4 2 0 20 Number of individuals Number of individuals Hours Hours 15 10 5 0 20 15 10 5 0 100 80 60 40 20 0 12 10 8 6 4 2 0 8 6 4 2 0 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 Strumigenys saliens Cerapachys sp.

Octostruma rugifera Rogeria sp.

Solenopsis sp.2 Stigmatomma armigerum 5 4 3 2 1 0 3.0 2.5 Number of individuals 2.0 1.5 1.0 0.5 0.0 4 3 2 1 0 4 0 5 10 15 4 3 2 1 0 3 2 1 0 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 Hours 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06 06:07 07:08 08:09 09:10 10:11 11:12 12:13 13:14 14:15 15:16 16:17 17:18 18:06

Fig.4. PhenologiesofflightactivityofcommonspeciesofaNeotropicalantassemblageinAtlanticForest,southeasternofBrazil.Phenologiesarethepooledactivityfrom

9 8 7 6 10 11 12 13 14 15 16 17 18 Hypoponera distinguenda Hypoponera sp.6 Pachycondyla sp.1 Stigmatomma armigerum Octostruma rugifera Cerapachys sp. Pheidole sp.4 Solenopsis sp.2 Hypoponera sp.1 Hylomyrma reitteri Rogeria sp. Solenopsis sp.1 Pheidole sp.5 Hypoponera sp.5 Acropyga goeldii Strumigenys saliens Hypoponera trigona Acanthognathus rudis Acanthognathus sp.

Fig.5.Phenologiesofflightactivityforallspeciesrepresentedbyeightormorespecimensintotal.Speciesaresortedontheverticalaxisaccordingtotheponderedaverage

ofhourofflight,producingtheobserveddiagonalizationfromearlymorningontoptonocturnalonthebottom.Frequenciesarenormalizedfrom0.0to1.0.

antfaunaintheAtlanticForestbiome(SilvaandBrandão,2010); further,Malaisetrapsmaycapturealateformsofthespeciesliving indifferentlayersoflitterandsoil,aswellasspeciesrestrictedto vegetation(Casta ˜no-Menesesetal.,2009).Indeed,Malaise trapp-inghasbeensuggestedasanefficientmethodtocaptureants(in particular,thearborealfauna)andinsomeapplicationscouldbea substituteforcanopyfogging(LonginoandColwell,1997).

Previousstudiessuggestthataconsiderableproportionofthe antspeciespresentsnocturnalnuptialflights(Kasparietal.,2001a;

Nascimentoetal.,2004),andthatthisbehaviorcouldbea

strat-egytoavoiddiurnalpredatorsandtheriskofdesiccationcausedby hightemperatures(Nascimentoetal.,2011;Torresetal.,2001). Also, the crepuscularhourswould be less windy thandaylight hours,andthereforemorefavorabletotheflightofsmallinsects,as

Table2

ClusteringoftimeofflightactivitybasedonallavailabledatabasedonunweightedarithmeticaverageandJaccard(binnary)

coefficient.Stabilityanalysis:foreachnumberednodeintheoriginaltree,itisshownwhichpercentageof30treesgenerated

byJackknifehadanequivalentnode.Twointeriornodes(indifferenttrees)areequivalentiftheyhavethesamesamples

asdescendents.

Tree Topology

Distance

_{analysis (%)}

Stability

+----06:00-07:00

1'

0.9344

4

10

0

| +----07:00-08:00

| +---

-5'

0.5000

0

97

| | +---

-08:0

0-09:0

0

| +---

-3'

0.6219

4

10

0

| | | +---

-16:0

0-17:0

0

| | +---

-6'

0.2500

0

10

0

| | +---

-17:0

0-18:0

0

+---

-2'

0.7607

1

10

0

|

+---

-09:0

0-10:0

0

|

+---

-11

'

0.4444

4

87

| |

+---

-10:0

0-11:0

0

|

+---

-9'

0.5189

4

97

| |

+---

-11:0

0-12:0

0

|

+---

-7'

0.6619

0

67

| |

+---

-15:0

0-16:0

0

+---

-4'

0.6739

4

97

|

+---

-12:0

0-13:0

0

+---

-8'

0.5849

3

93

|

+---

-13:0

0-14:0

0

+---

-10

'

0.5000

0

10

0

+---

-14:0

0-15:0

0

ants(Baldridgeetal.,1980).Contrariwise,thisstudyfoundthata smallproportionofspecieshadnuptialflightsduringthenight,and thatdiurnalflightsaccountforanimpressive95%oftheantflight activity.IntheAtlanticForestofsoutheasternBrazil,thevariation oftemperature,moisture,and windspeedbetweendiurnal and nocturnalperiodsislesspronouncedthaninopenerand/ordrier tropicalbiomes(Vieiraetal.,2015),whichcouldhelptoexplainthe highnumberofdiurnalflights.

Ithasalsobeensuggestedthatnocturnalpredatorssuchasbats, frogs,nocturnalwasps,andothers,canalsocausesignificantlosses duringantnuptialflights(Levinetal.,2009).Thiscouldbesomehow relatedtothescarcecatchingsinnocturnalsamples,butalso rep-resentsaselectivepressurethatspeaksinfavorofdiurnalflights.In addition,ourresultssuggestthatspecieswiththickestintegument (i.e.,Dorylinae,Myrmicinae,andPonerinaeantsinthisstudy)may extendtheflightperiodforseveralhoursalongtheday,including thehottestperiods,whichmightpossiblyberelatedtoahigher abilitytoreducewater loss.Torres etal.(2001)alsofoundthat queensstarttoflyearlierinthedaythanmales,andthatcould explainthelownumberofmalesinthepre-dawnperiod(04:00to 06:00h).

Malaisetrapswereextraordinarilymalebiasedinthisstudy, andthisisconsistentwithotherneotropicalantassemblage sur-veys(e.g., Kaspari et al., 2001a,b) and taxonomic studies (e.g.,

YoshimuraandFisher,2012).Oursamplingdesignwithdataon

flightsatspecifictimesofthedayalsoprovidedstrongevidenceof ahighdiversityinphenologyforantspeciesintheAtlanticForest, eventhoughmostspeciespresentedhighlyasynchronous inter-specificflights.Nuptialflightsynchronizationhasbeenassociated withpredatoravoidance,maintenance of reproductiveisolation andoutbreedingpromotion(Torresetal.,2001).

Asdescribed in other studies on the neotropical ant fauna, flightsofDorylinae,Formicinae,Myrmicinae,andPonerinaemay occur at equal times of the day (Kaspari et al., 2001a; Torres et al., 2001).Species of other typicalNeotropical ant subfami-liesasDolichoderinae,ProceratiinaeorPseudomyrmecinaewere absentinourMalaisesamples,but thismaynotbe straightfor-wardlyrelatedtosamplingefforts.Dolichoderinae,forexample, includesspeciesinwhichnuptialflightscontainfewindividuals

(Torresetal.,2001).Inaddition,leaf-littersamplingatBBS

sug-geststhatDolichoderinaespeciesarenotcommoninAtlanticForest

(SilvaandBrandão,2010).

Thisstudyisthefirsttoinvestigateflightpatternsalonga24h timerangeforanantassemblageinthetropics,anddespite repre-sentingonlya5-daysnapshot,relevantfindingsemerged.Ahigh speciesrichnesswasfoundatthestudysite,andmalesofthe sam-pledsubfamiliesprobablyprefertohavenuptialflightsduringthe day.FlightactivityofantmalesatBBSfallintothreegroups:sunrise, sunset,andflightsduringmostoftheday.Similarityanalyses, how-ever,suggestthatcloselyrelatedtimerangesofflightactivitymay actuallynotbecontinuous(Table2).Thismightmakesense,since climaticfluctuations along daytime are approximately bimodal (morning/afternoon).Thisisfurthersupportedbytheaggregations ofmalesofdifferentspeciesofthemostfrequentantgenusinthis study,Hypoponera,observedatdifferentperiodsoftheday, sug-gestingstaggeredflightsofcongenericspecieswithinthenarrow rangeofasinglehouroftheday.

Finally,somespeciesseemtoshowaclearlypulsedflight activ-ity,happeningatdifferentperiodsoftheday.Overall,thisstudy revealsarich,perhapsevensurprising,diversityofflight phenolo-giesforAtlanticForestants.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

We acknowledge support from the Fundac¸ão de Amparo à PesquisadoEstadodeSãoPaulo(FAPESP)withresearchgrantsto R.R.Silva(Processes10/20570-8and10/51194-1)andR.M.Feitosa (Process 07/01310-2), and the Conselho Nacional de Pesquisas (CNPq)witharesearchgranttoA.P.Aguiar(Process926.656.810). LianaKonnoNogueiraandJulianaColiSouzawerepartofthefield teamwhichconductedtheexperiments,andtheirparticipationis appreciated.

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,atdoi:10.1016/j.rbe.2016.05.006.

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