Influence of soil granulometry on average body size in soil ant assemblages : implications for bioindication.

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SupportedbyBotic´arioGroupFoundationforNatureProtection

www.perspectecolconserv.com

Essays

and

Perspectives

Inﬂuence

of

soil

granulometry

on

average

body

size

in

soil

ant

assemblages:

implications

for

bioindication

Cinthia

Borges

da

Costa-Milanez

a,∗

_,

_Jonathan

_D.

_Majer

b,c

_,

Paulo

de

Tarso

Amorim

Castro

d

_,

_Sérvio

_Pontes

_Ribeiro

a

a_Laboratory_of_Evolutionary_Ecology_of_Canopy_Insects_and_Natural_Succession,_Department_of_{Biodiversity,}_Evolution_and_Environment,_ICEB,_Universidade_Federal_de_Ouro_Preto,

CampusMorrodoCruzeiro,M.G.,Brazil

b_School_of_Biological_Sciences,_University_of_Western,_Perth,_Australia

c_Department_of_Environment_and_Agriculture,_Curtin_University,_Perth,_Australia

d_Department_of_Geology,_Universidade_Federal_de_Ouro_Preto,_Campus_Morro_do_Cruzeiro,_M.G.,_Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received29November2016

Accepted31March2017

Availableonline26June2017

Keywords: Mining Rehabilitation Veredas Wetland Soiltexture

a

b

s

t

r

a

c

t

Soilgranulometriccompositioncanimposeconstraintsonantspecieslivingingroundhabitats,being animportantfactorindefiningthehabitattemplet,whichdescribeshowcertainanimallifehistories, includingthetraitofbodysize,canbeselected.Theantfaunaplaysacentralroleinsoilformation,and avastliteraturedescribessuchinfluence,butnottheconverse.Alongwithtermites,wormsandother invertebrates,theseorganismspromotetheformationofchannels,pores,andaggregatesthatinfluence gasesandwatermovingthroughthesoilprofile.Ontheotherhand,itisimportanttounderstandwhether soiltraitsconstraininsectcolonization,sowehereaskhowsoiltraitscaninfluencenichespecificities, whichseemstobeaneglectedecologicalissue.Aliteraturesearchusingthekeywords‘antsorFormicidae’ and‘soilstructureorpedogenesis’revealednumerousreferencesdealingwiththeinfluenceofantsonsoil, butnotconversely.Weherepresentanovelgeomorphologicapproachtohabitattempletsfortwodistinct riparianNeotropicalecosystems,basedontheamalgamationofsoil/sedimentanalysiswithecological processesandantspeciesbiology.Wefoundthatpredominanceoffinegrainsfavouredthepreponderance ofsmallantspeciesatathresholdof<5mminbodylength.Basedonthis,weproposetheuseofa quantitative,theoreticallysound,statisticalapproachtobioindication.

Introduction

SinceHutchinson’sclassicalconsiderationofevolutionasaplay performedintheecologicaltheatre(1965),ecologistshavetriedto incorporateanytypeofrolewithinthespeciesandforcingan adap-tativeexplanation,notalwaysvalid,totheirinteractions.However, whetherneutralandrandom(Strongetal.,1984;Hubbell,2001),or aproductofdirectionalevolutionaryforcesimposedby interspe-cificcompetition(CodyandDiamond,1975’sfirstandsecondrules ofcompetitionandcommunitystructuring),speciescomposition andspeciesrelativedensitiesarefingerprintsoftheenvironment. As such, species and population traits may lead to a practical use,namelybioindicating theexistenceofcertainconditions in ecosystemsortheirhabitats.It followsthatspecies community

∗ Correspondingauthor.

E-mailaddress:[email protected](C.B.Costa-Milanez).

parametersshouldreflectecosystemhealthandintegrity.The base-lineforthisapproachcomesfromSouthwood’s(1977)Presidential Address to the British Ecological Society, when he speculated whetherhabitatwouldbethe“templetforecologicalstrategies”. Inotherwords,heelegantlyexplainedhowhabitatsconstrainand definewhatkindofcommunitymustbefoundinthem,basedon speciesspecificities.

FurtherexploredbyGreenslade(1983),thehabitattemplet con-ceptwasusedtobetterexplainlifehistorydistributionsinnature, andwasreﬁnedtoasimplisticr-tok-toA(forAdversity)strategies triangle.Thistheoreticalframeworkshouldbeanobvious foun-dationfortheconceptofbioindication,sincebymonitoringwhat speciesarefoundincertainhabitats, onecouldprovide arapid diagnosisofimpactsonthesehabitats.Theabsenceofexpected species,orthepresenceofopportunistic,unexpectedspeciesare bothfactsrelatedtodisturbance,andthemonitoringofsuchspecies forbioindicationislikelytobecheaperandquickertocarryoutthan afullenvironmentaldiagnosis.

http://dx.doi.org/10.1016/j.pecon.2017.03.007

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Despitethispromisingidea,theprinciplesofthehabitat tem-plethavenotbeenwidelyadoptedasbaselineforappliedstudiesof speciespopulationsorcommunities,exceptinthecaseofbenthic aquaticfauna(MarquesandBarbosa,2001;Marques,2004).There aretwopossiblereasonsforthis.Ontheonehand,theideaofa habitattempleterroneouslyassumesconstancyintheabiotic con-ditions,anddoesnotconsiderthecountereffectof,forinstance, howaspeciescanchangethehabitatduringnaturalsuccession. Neitherdoesitconsiderwhichspeciescausethemostdeﬁnitive changesinhabitatconditions(Jonesetal.,1997).Weacknowledge thatthedifﬁcultyofobtainingdataonabioticandbioticmatching conditionsrendersadirecttheoreticalapproachlesspalatablefor appliedecologists.Still,noneoftheseimpedimentsshouldhinder attemptstoincorporatethehabitattempletconceptinto bioindi-cationprocedures.

Membersofthesoilfaunaareamongthemostdiverse com-ponents of an ecosystem (Vargas and Hungria, 1997). The soil macrofauna,includingants,spiders,termites,earthwormsand oth-ers(Bachelier,1978;Berthelinetal.,1994;Lavelleetal.,1994)are representativesofkeyfunctionalguilds.Throughdigging,foraging, buildingnests,galleries,chambersandcorridors,ortransporting excavatedsoilmaterials,theyredistributeorganicandinorganic matteracrossthesoilproﬁle.Itfollowsthatthemacrofaunacan beusedasabioindicatorofsoilquality,sinceitplaysan impor-tantroleintheregulationofpedogeneticdevelopment(Brussard, 1998).

Likewiseinaspecies-engineering(Jonesetal.,1997)ora habi-tattemplet(Greenslade,1983)approach,ants,amongstalltaxa, oughttobetakenintoaccountwhenconsideringsoiltraitsthat selectspeciesoccurrence.However,soilfaunaisnotalways consid-eredinstudiesofsoilbeyondadescriptionofcommunitypatterns (Andersen andMajer,2004).Indeed,asfarasweknow,beyond ourworkonlyYanoviakandKaspari(2000)consideredantspecies traits(namelybodysize)basedonhabitattempleteffectson com-petitionbetweenspecies.Notwithstandingthis,invertebratesare widelyusedinimpactandenvironmentalrestorationstudies, espe-ciallyinabioindicativeapproachtohumanimpacts(Abbottetal., 1979;Majer,1983;Pérèsetal.,2011;Simmonsetal.,2015).

Weherereviewdisturbanceinsoilstructureandtheusageof antassemblagesasbioindicationtoolsfordiagnosingchangesin habitats.Then, we illustratetheuseofsuchanapproach using twoBrazilianexamplesofantassemblageresponsetosoilimpacts. Finally,wediscusstherelevanceofadoptingatheoreticalapproach forappliedsoilecologystudies,basedontheassumptionthatsoil granulometryisakeyhabitatﬁlter,andthusacomponentofthe habitattempletforsoilfauna.

Disturbanceandsoilstructure

Thesoiloriginatesfromrockdegradingprocessesorstructural rearrangementofapreviouslytransformedmatterthatcomposes theearth’ssurface(Castro,2008).Thesechanges arecaused by chemical,physicaland biologicalfactorsthatinﬂuencetherock matrixandcausesoilhorizonshaping,andthus,heterogeneitydue tovariationsinmineralogicalcomposition,colour,texture,and/or structure(BeljavskisandJuliani,1986).

The mineralportionof the ground is composedof particles of various dimensions and arrangement in space. These sands, mudsandgravelscompriseindividualparticlesthat,along with organicmatter,airandwater,constitutewhatweknowas‘soil’. Determiningthegranulometricdistributionof sizeand propor-tionsofconstituentparticlesisthebasisforaccuratedescription ofsoils.Thesetraitsdirectlyaffectphysicalprocessestakingplace in soil, such as transport and deposition, porosity and perme-ability(Suguio,1980).It isthroughknowledgeofgranulometric

distributionthatonecaninferaboutthepotentialforcompaction, aeration,transmissionofheat,inﬁltrationandwaterdistribution insoil(Prevedello,1996).Soiltraitsrelatedtowaterretentionand nutrientavailability toplantsaremajorcomponentsofedaphic stratiﬁcation(Silvaetal.,2005)andareessentialforthediagnosis ofsoilfunctioningaswellaseffectsofdisturbance.

Variousdistinctsoilfeaturesmayappearafterdisturbance.Soils thathaverecentlybeenexposedorimpactedbyactivitiessuchas miningmayhaveahighinﬁltrationcapacity,sincetheirgrain struc-turebecomesdisarranged.However,ifexposedforalongperiod, soilaggregatesarebrokenupbythekineticenergyofraindrops whentheytouchthesoilsurface.Theseseparatedparticlesmay formadensecrustafewmillimetresthickonthesoilsurface, fur-therreducinginﬁltrationofwater,transmissionofheatand gas exchangebetweensoilandatmosphere,andalsoimpacting nutri-entcycling(Al-DurrahandBradford,1982;LeBissonaisetal.,1989). Thecompactionprocessresultsindecreasingroughnessand vol-umeofmacropores,thusincreasingthedensityofthesediment (Leiteetal.,2004).Soilmacro-andmicronutrientsatthesurface becomeblockedbythethinand compactcrustandwillnot be washed downtothedeeperlevels.Due tothis process,during therainyseasonnutrientsareleachedandovertimetheprocess mayresultinsoilnutrientimpoverishment,whichleadstoslow orstagnatednaturalsuccession,anissuethatmayimpedehabitat restoration.

In disturbed areas, ants contributeto soil recovery, as they promote changes in chemical and physical properties, making soilsricherin availablenutrientssuchasnitrogen,phosphorus, potassium,magnesiumandcalcium(CarlsonandWhitford,1991; Wagneretal.,1997;Lafleuretal.,2005).Furthermore,theymix soilgrainsbythebioturbationprocess(Hole,1961;Lavelle,1993; Pielström and Roces, 2013). The galleries formed by ants are particularlyimportantinenvironmentalrecovery,evenafterthe colonyhasbeenabandoned.Thenetworkofgalleries(orbiopores) connecting nest chambers has a significant influenceon water infiltration,onsoilaerationprocessandonrootpenetration, par-ticularlyinareaswheretheupperlayerofthesoiliscompacted (LobrydeBruynandConacher,1994;Nkemetal.,2000).In ecosys-temrehabilitationprojects,suchasafterminingorothersevere typesoflongtermdisturbance,antsoccupyanimportantroleinthe regulationofvitalprocessesinsoil,creatingchannels,pores,and aggregates(Coutinhoetal.,2003;Lavelleetal.,2006),increasing fertilization(Wuetal.,2013)andcausingprotectionfromerosion (Hawksworth,1991;Doranetal.,1994).

Bioindicationbyants

Changes in natural habitats maybe detectedby monitoring bioindicatorspeciesorfunctional guilds,which consistofthose populations(orassemblagesofspecies)thatreflectthe conserva-tionstatusofthebioticandabioticenvironment.Inotherwords,a taxonomicbioindicatorgroupcanreflectchangesinimpacted habi-tats,communitiesorecosystems,astheirecologicalrequirements change.Themoretheyarerepresentativeofoverallcommunity diversityandofdistinctecologicalfunctions,thebetterindicators theyare(McGeoch,1998).Antsareconsideredexcellent bioindica-torsbecausetheyareanextremelyabundantgroup,withrelatively highnumbers of speciesthat are taxonomicallytreatable, with many specialist species occupying different trophic levels and niches,andmanyofthosespeciesreactpromptlytochangesin theenvironment(Majer,1983).Antdiversityisinfluencedbythe diversityanddensityofplantspecies(Bassetetal.,2012;Queiroz etal.,2013),vegetationphysiognomy(especiallystratification–

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temperature,humidity,andsoilcomposition(Cardosoetal.,2010; Costaetal.,2010;Philpottetal.,2010).

Theconceptofbioindication,though,hasnotbeenconsidered inrelationtootherecologicaltheories,someofwhichareessential fordeﬁningaproperroleofspeciesinacommunity.Inorderto reachabioindicativeconclusion,onemustdelimitacertainsetof habitatconditionsintowhichseveralnichescanbeaccommodated, thusproducingatempletofhabitatswherecertainspeciesshould befound(Southwoodetal.,1974;Greenslade,1983;Yanoviakand Kaspari,2000).Forinstance,thelackofexpectedspeciesor func-tionalguildsprobablyindicatessomeunperceivableimpactthat mayhaveremovedthosespeciesfromtheirpositioninthe tem-plet.Hence,not justtohavesomespecies, buttohave themin greaterorsmallerdensitiesthanexpected,ortobenotthereatall, arewaystocharacterizeanimpactedecosystem.

Furthermorethough,itisnecessarytoconsiderthefunctional roleofthesespeciesandguilds.Ants,forinstance,serveperfectlyto illustratetheconceptofengineerspecies,ascoinedbyJonesetal. (1997).Thesequalitiesas‘engineers’makeantassemblages impor-tant componentsfor buildingbioindication tools.In this sense, soil-dwelling ants ought tobe considered when attempting to understandsoil protectionor restoration after impacts suchas thosecausedbymining.Morethanjustreﬂectinggoodorbad con-ditionswithinahabitat,antswillchangesoilhabitatsintoabetter successionalstate,andthusarealsopredictablecausesofchanging directionsinthequalitativestateoftheecosystem.

Manystudieshaveusedantsasbioindicatorsofnatural suc-cessionafterhumanimpacts,suchasmining(Majer,1983,1984; MajerandNichols,1998),soilcontaminationbymetals(Ribasetal., 2011),establishmentofEucalyptusmonocultures(Costa-Milanez etal.,2014),ornaturalimpactsincludingﬁreinthecerrado,which hasincreasedinfrequencyoverrecentyears(Frizzoetal.,2012; Cautetal.,2014;Andersenetal.,2014;Calcaterraetal.,2014;Anjos etal.,2015;Costa-Milanezetal.,2015).However,mostofthese studieshavenotdealtwithhowthegrounddwellingant assem-blagesareaffectedbyimpactsonsoilphysicaltraits,suchastexture. Thenextsectionexploreswhatispresentlyknownonants’species responsestosoiltraitsinnaturalconditions,andpresentsourmost recentresultsonhowsubtlesoilchangescausedbyimpactscould beassessedbasedonsoilantspeciesrelativedensities.

Howsoilmodiﬁcationcanaffectantassemblages

Twoof our studies, one in riparian vegetationimpacted by dredgingintheJequitinhonhaRiverbasin, andtheotherinthe ‘veredas’wetlandsintheBrazilianSavanna,haveinvestigatedhow soilgranulometricdistributionafterdisturbanceaffectsthe pres-enceofants.(Costaetal.,2010;Costa-Milanezetal.,2014;PhD unpublisheddata). Inboth studies,wefoundasignificant posi-tiverelationshipbetweentheproportionoffineandveryfinesand grainswiththedensityofsmallants(antspecieswithabodysize smallerthan5mm).Here,wedeveloparationaletosupportthe hypothesisthatantbodysizeisalifehistorytraitthatislikelyto beusefulforthebioindicationofsoilqualityandecological succes-sion.

Soilantnestandsubterraneangalleryconstructionare inﬂu-enced by the ability to extract soil particles with the ant’s mandibles, legs and psammophore (in some members of the Dolichoderinae,FormicinaeandMyrmicinae),astheycarrytheload takenfromthesoiltoanotherplace(Fig.1D).Camponotus punc-tulatusMayr1868,forexample,canrelocate2100kgha−1ofsoil duringtheconstructionprocessofitscolonymounds(Folgarait, 1998),andAttasexdensLinnaeus1758constructsitsnestoveran areaofapproximately100m2_,_occupying_a_volume_of₂₃_m3_,_with

almost40tonnesofsoil(Autori,1947).

However,iflarge-bodysizedsoilants,suchasC.punctulatusand A.sexdens,arefavouredbycoarsegrains,thesamemaybenottrue forsmallsizeants,unabletomanagelargefragments.Ontheother hand,byhavingverysmallbodysizes,someantspeciescould bene-fitbytheirpotentialabilitytocollectsomehard-to-findresources, aswellastohidefromharshmicro-climaticconditionsin shel-tersfoundamongtheinterstitialspacesofasandy,veryfinesoil (KaspariandWeiser,2007).Besides,duetofinesoilconstraining traitsagainstthepresenceandmovementoflargeantspecies,this veryspecifichabitatcomponentmayresultinanenemy-freespace tothesmallantspecies.

Thesoilisnormallycoveredwithleaves,twigsandother obsta-clesthatcanleadtotheformationofacomplexthree-dimensional environment(YanoviakandKaspari,2000).Antswithlargebody sizescancrossobstaclesmoreeasilythanantswithsmallbody sizes,andthelattermayeventuallychoosetomaketheirjourneys throughthesubterraneaninterstitialspaces.Therefore,largeants usuallyrecruitforforaginginthelitter,whilesmallantsrecruitfor foraginginthechannelsbuiltinthegroundandunderneaththe litterfoundincertainhabitats(Costaetal.,2010).

Therelationshipbetweensoiltextureandantbodysizenotonly influencestheprocessofnestfoundationandestablishmentin cer-tainsoiltextures,asdiscussedinKaspariandVargo(1995),butalso influencesthesurvivalrateofcolonies.Soilswithahighclay con-centrationhavehighercapacitytoretainwater,reducingtheriskof desiccationofants.Intheearlystagesofthecolony,desiccationis oneofthefactorsthatresultsincolonymortality(Johnson,2000). IntheJequitinhonhaRiverstudy(Costaetal.,2010),whichwas undertakeninatransitionalareafromBraziliansavanna(cerrado) to semi-arid deciduous forests, the region also contains semi-deciduousforests(Fig.1Aand B).A diamond miningcompany dredgedthebedandbanksoftheupperbasinoftheRiverover adistanceof11km.Beforedredgingthesedimentbed,thesurface soilwassavedfor lateruseinrestoration. Riverbanksare cov-eredwithseveralnativetreeandshrubspecies,suchasPilosocereus gounellei(xique-xique),Acaciaalata(acacia),Tabebuiachrysotricha (ipê amarelo) and Solanumsp., amongst others (Ribeiro, 2002). Between1991and1995arestorationprojectwasimplemented inthestudyareaand10yearslaterweselectedsevenlocations withintherestoredsitesandtwoundisturbedareas(controls)to investigatetheeffectofsedimentarygrainsizeonantspecies diver-sityand abundance.AntsamplingwasconductedinApril2005, usingthreemethods,namelybaits,pitfalltraps,andhand collec-tions.Anincreaseintheproportionofsmallantspeciesof5mmor lessbodylengthwiththeincreaseinpercentageoffinegrainsin thesedimentwasobserved(Fig.2A–TableS1).Thisrelationship veryneatlyexplainedthedisproportionateoccurrenceofworkers ofsmallspecies,suchasDorymyrmexpyramicusRoger1863,but thepredominanceoffinegrainsdidnotexplainoverallantspecies richnessandabundance.Dorymyrmexpyramicusistypicalofopen environments,impactedareasandislesssensitivetohuman dis-turbance(Santosetal.,1999;Costaetal.,2010).Thezoneswhere this species dominated had a slow rehabilitation recoveryrate becauseof theirproximitytoJequitinhonhariver,which suffers fromthedirectinfluenceoffloodsduringtherainyseason(Costa etal.,2010).Theeffectsoffloodingweresignificantbutwerealso confoundedbytheunderground waterlevel,whichmayinhibit treerootdevelopmentandantcolonization.

Thisresult highlights a problemin the restoration methods usedafterdredging.Therelocationofalluvialsedimentsresulted inlargechangesinsoilgranulometricmakeuptoastatethatwas quitedifferenttohow it wasbeforethe dredging(Costa etal., 2010).Mostofthegrainsin therestorationareawerebetween 0.2and0.06mm(ﬁnesandandveryﬁnesandclasses)andwere largelycomposedofquartz.Thevariationinantspeciesamongthe studiedareascouldindicateadifferentiationinthedistributionof

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Fig.1.SectionfromtheJequitinhonhariverinrehabilitationpostmining(A),rehabilitationareaneartocerrado(B),veredawith5-yearoldEucalyptusplantation(C)and

Attasexdenscarringsoilgrainswiththemandible(D).

resourcesandhabitatstructure,whichconformstooursuggested habitattemplet-nicheresponsepattern(Southwoodetal.,1974; GreensladeandGreenslade,1984;YanoviakandKaspari,2000).In particular,granulometriccompositionandsoilstructureseemsto favourforagingandnestingbydifferentsizedants(Farji-Brener etal.,2004).Becauseofthis,ifcertainsoilconditions constrain antcolonization,anegative feedbackprocessmay resultinthe furtherstagnationof succession.Examplesof antsfoundinthe studythatwereabsentinsoilswithsubstantialaccumulationof ﬁne sand quartzes include Atta sexdens rubropilosa Forel1908, NomamyrmexesenbeckiiWestwood1842,andEctatomma permag-numForel1908.BothA.sexdensrubropilosaandN.esenbeckiiwere sampledinundisturbedareasandtheformerspeciesrequiressome preservedandstructuredsoiltomaintainthecolony(Moutinho etal.,2003).Furthermore,itformsthemaindietarycomponentof N.esenbeckii,whichisasubterraneanspecies(SouzaandMoura, 2008).Ectatommapermagnumisanaggressiveepigaeicpredator thatbuildssmallnestsinsoil(Brandãoetal.,2012).Thenesting behaviouroftheselargeantsisunderground,sotheproportion ofﬁnegrainsandthefactthatgroundwaternearthesurfacemay notfavourcolonizationistheseenvironments,thusimpedingthe developmentofamorecomplexfoodweb.

Intheveredaswetlandsstudy,Costa-Milanezetal.(2014) inves-tigated theresponse of antspecies to changes in wetland and cerrado‘sensustricto’soilafterintroductionofEucalyptus monocul-ture.TheBraziliansavanna(cerrado)wetlands,socalledveredas, areheadwatersofshallowdrainages.Thisecosystemisformedon sandysoilswithhighconcentrationsofpeat(Eiten,1994; Alencar-Silvaand Maillard,2007), andis composedof soilsofveryﬁne particlesizewhichiswellstructuredandchannelledduetolarge amounts of decaying organic matter. These characteristics cre-atewet,blacksediment thatiscolonizedbyhydrophilicgrasses (Fig. 1C). However, during the years 1970–2000, 44% of natu-ral Brazilian savanna, including that surrounding veredas, was

replacedbyEucalyptusmonocultureplantations.Suchplantations tend toworsen thelocal water deficit,soil fertility and pH,as wellasdecreasingnativefaunabiodiversity(Souzaetal.,2006; AlcidesandPereira,2007).Thefieldworkwascarriedoutintwo reasonablywell-preservedveredas(controllocations)andintwo disturbedveredas(modifiedlocations:onesurroundedbya3-year oldEucalyptusplantationand othersurroundedbya 5-yearold Eucalyptusplantation).AntsamplingwasconductedinMay2010 (dryseason) usingthree methods, namelybaits(soiland arbo-real),pitfalltraps(soilandarboreal),andhandcollections.Inour study,therewasaclearcontrastbetweenareaswithgreater pro-portionsofcoarsegrainsoil(inwetlands)versusareaswherefine grainsnaturallyoccur(finesandandveryfinesand),suchasin Eucalyptusandcerradohabitats(Costa-Milanezetal.,2014).Here, asignificantpositivecorrelationwasfoundbetweenthedensity of small antspecies in areaswhere theproportion of fineand veryfinegrainswasdetected(Fig.2B–TableS1).This relation-shipexplainedtheoccurrenceofsmall,oftenaggressivespecies inthecerrado,suchDorymyrmexjheringiForel1912and Solenop-sisinvictaBuren1972,alongwithadisproportionateoccurrence ofPheidolegertrudaeForel1886intheEucalyptushabitats. Appar-ently,thenaturalgranulometriccondition,whichisatempletfor smallants,couldbedisturbedafterplantationestablishment,thus intensifyingitsfilteringeffectontheantspeciesassemblage.This modification allowedlargecolonies of the mostaggressive ant species, suchasSolenopsisinvicta and LinepithemahumileMayr 1868,tocolonizetheseareaswhich,asaresult,lowerantspecies diversity.

The whole process of preparing the plantation promotes changesthatmaybefavourableforsomespeciesbutnotforothers. Antsofapproximately5mminsizeorlesswerefavouredinareas withahigherproportionofﬁnegrains,asexempliﬁedbyP. gertru-daeintheEucalyptushabitat.Overtofouryearsofstudy,69%of sampledantsbelongedtothegenusPheidole.Thesmallbodysized

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A

1 0.8 0.6 0.4 0.2 0 75 65 55 45 35 25 0 10 y = 0.005x + 0.2769 R2 = 0.2058 y = 0.3285x + 37.528 R2_{= 0.5233} 20 30 40 50

Percentage of fine sand sizes

Proportion of ants species size

≤

5 mm

Proportion of ants species size

≤

5 mm

60 70 80 90 100

0 10 20 30 40 50 60 70 80 90 100

B

Fig.2. Simplelinearregressionontheproportionofantspecieswithbodysizeupto5mmasafunctionoftheproportionofﬁneandveryﬁnesandgrainson(A)riparian

vegetationimpactedbydredgingintheJequitinhonhaRiverand(B)veredaswetlands.

antspeciesofthisgenusnestindiverselocations,includingsoil, litterortrunks,andhavelargecolonieswithmassiverecruitment (Lizidatti,2006).Allofthesecharacteristicsmakethemeffectivein colonizingvacanthabitatsandexcludingcompetitors.Indeed,the dominanceofthis specieswasdisproportionate,indicatinghigh disturbance.

In contrast,some authorshave foundthat wetland habitats hadless ﬁnegrainsdue totheaccumulationoforganicmatter. Theorganicmaterial makesthesediment/soillumpy, maintain-ingthemoistureinthespacesbetweenthegrains.Thesegranules formagglomeratesbytheprocessofagglutination,orby contrac-tion/relaxationofsoilmuds.Curiously,inmorematureEucalyptus monocultures,thesoiltendstoevolveintothisdirection,andthis processisfurtheraccentuatedbythereductioninthegroundwater level,whichresultsinmoreandbiggeragglomerates(Viana,2006; Melo,2008).Asaresult,plantationsestablishedoncerradosoilswill endupwithastructuremostunlike,andcoarserthantheoriginal. Afterasubstantialperiodoftime,thenumberofsoilantspeciesand theaverageantsizemayincreaseinEucalyptusplantationsbut,in thiscase,thisindicatesafurthersoilchangetowardsaevenmore distinct,althoughmorediverse,habitattemplet.Thepossibilityof usingthesameassumptions ofniche-habitatadjustmentsbased onthehabitattempletmodeltodetectnovelecosystemsseems toustobeanevenstrongerargumentinfavourofestablishing aserioustheoreticalfundamentwhileapplyingthebioindication concept.

Concludingremarks

Herewe havepresentedresultsfromtwoindependent loca-tions,sothegeneralitiesofwhatwearesuggestingneedfurther investigationinotherhabitats andPalaeo-regions(forinstance, Australasianantfaunamaynothavesuchsmallspeciesin oppor-tunisticguildswithdominantabundances,andRhytidoponeramay replaceBrachymyrmex).However,wesuggestthatacompleteor partialchangeinthesoil/sedimentparticlesizeisanimportant determinantoftheantspeciesdistributionpatterns,whichcould thereforebeusedasatoolforthebiomonitoringofdegradedareas, atleastforriparianandecotoneforest-freshwatercommunities. Further,thedatadiscussedheremayclarifythepotentialforusing antsasbioindicatorsinprocessesofchangeinsoiltexturein var-ioussituations, asdiverseasminingand plantingof Eucalyptus monocultures.However,it isimportanttonotethatthistool is fundamentallyecological,andisthereforequantitativeand the-oreticallysound.Animportantaspectfortheconstructionofthis analyticaltoolistheamalgamationofsoil/sedimentanalysiswith ecologicalprocessesandantspeciesbiology.Also,weseeanurgent needtoconsolidateadeeper,theoreticallysoundapproachtothe useofbioindication.Thisurgencyhasimplicationsforthe increas-ingunpredictabilityintheclimateandlandusechange.Likewise, quitespeciﬁcally for theMinas Gerais Statewhere these stud-ieswereconducted,thereisanurgencytoimprovebioindication toolsasaresponsetotherecentworstriverdisasteronEarth(the

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Samarco’smudﬂoodonthewholeDoceriverbasinuntilthesea), traversingthisandalsoEspiritoSantoState.

Conﬂictofinterest

Theauthorsdeclarenoconﬂictsofinterest.

Acknowledgements

WethankRodrigoFeitosaforidentifyingtheantssampledin thisproject.Twoanonymousreferees,plusGrazieliDueliandBrian Heterickimprovedthemanuscript.TheFinancialsupportforCB Costa-MilanezwasprovidedbyConselhoNacionalde Desenvolvi-mentoCientíﬁcoeTecnológico,CNPq.SPRibeiroandPTACastroare grantedresearcherbyCNPq.IBAMAprovidedthecollectpermits.

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,atdoi:10.1016/j.pecon.2017.03.007.

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