Trophic network of aquatic macroinvertebrates along an altitudinal gradient in a Neotropical mountain river

REVISTA

BRASILEIRA

DE

Entomologia

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

Biology,

Ecology

and

Diversity

Trophic

network

of

aquatic

macroinvertebrates

along

an

altitudinal

gradient

in

a

Neotropical

mountain

river

Cesar

E.

Tamaris-Turizo

_,

_Gabriel

_A.

_Pinilla-A

_,

_Isabel

_{Mu ˜}

_noz

a_{UniversidaddelMagdalena,GrupodeInvestigaciónenBiodiversidadyEcologíaAplicada,SantaMarta,Colombia}

b_{UniversidadNacionaldeColombia,DepartamentodeBiología,GrupodeInvestigaciónenBiodiversidad,BiotecnologíayConservacióndeEcosistemas,Bogotá,Colombia} c_{UniversitatdeBarcelona,DepartamentodeBiologíaEvolutiva,EcologíayCienciasAmbientales,Barcelona,Spain}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received9February2018 Accepted22July2018 Availableonline2August2018 AssociateEditor:AdolfoCalor Keywords:

Aquaticinsects Foodchainlength GairaRiver Gutcontents Trophicrelations

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Studiesoftrophicnetworksandtheevaluationofprocessesthatoccuralongaltitudinalgradientsinriver systemsareofgreatimportancebecausetheyallowanunderstandingofenergyflowdynamicsand pro-videscientifictoolsfortheplanningandmanagementofriverecosystems.Thisresearchdescribesthe trophicnetworkofaquaticmacroinvertebratesalonganaltitudinalgradientoftheGairaRiver,a moun-tainNeotropicalwatercourselocatedintheSierraNevadadeSantaMartainnorthernColombia.The organismswerecollectedintheupper,middleandlowerreachesoftheriverduringtherainyanddry seasons(between2010and2013).Trophicrelationshipswereevaluatedthroughgutcontentanalysis. Thecontentsweredeterminedandquantifiedusingphotographsandexpertreview,andabinary con-sumptionmatrixwasusedtodeterminethecharacteristicsofthetrophicnetwork.Wecharacterizedthe dietcompositionateachsiteforeachseasonusingdiscriminantanalysis.Trophicnetworksduringthe dryseasonsshowedhighertrophicspeciesrichnessandlinkagedensity,andthepredominanceofcoarse particulateorganicmatter(CPOM)andfineparticulateorganicmatter(FPOM)inthehighandmedium sectionsoftheriver.Duringthedryseasonsthedietshadalowernumberofbasalspecies,butinthelow riversectiontherewasahighpercentageoffungiandmicroalgae.Duringtherainyseasons,nopatterns wereobservedforthepercentageofresources.Resultsindicatedadirectrelationbetweenperiodsof hydrologicstabilityandanincreaseofCPOMduringdryseasonsandanincreaseofresourcediversity consumedbymacroinvertebratesatallsitesduringtherainyseason,showingthatchangesintrophic networksoftheGairaRiverweremoreimportantduringseasonalperiodsthanalongthealtitudinal gradient.

©2018SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Macroinvertebratesconstituteanabundantgroupin freshwa-terecosystems.Theyplaya fundamental rolein thetransferof energythroughtrophicnetworks(AllanandCastillo,2007).Energy transferdependsmainlyonthediversity,qualityandquantityof resourcesavailablein thesystem,aswellas onthenumber of consumersand theirtrophic relationships(Merritt etal., 2008; Cumminsetal.,2005).Energytransferisevaluatedmainlythrough theattributesoftrophicnetworks(VanderZandenandRasmussen, 1999), which help to understand changes in trophic relation-shipsthatoccurduringvariationsinclimaticperiodsoratsites withdifferentenvironmentalconditions(Ruhíetal.,2016).Many

∗ Correspondingauthor.

E-mail:ctamaris@unimagdalena.edu.co(C.E.Tamaris-Turizo).

macroinvertebratesincorporateprincipallyallochthonousorganic matter(e.g.energythatisnotproducedlocally)thatcomefromthe riparianforestoristransportedfromupstreamandfromtributaries (Jackson andFisher,1986).Thissourceof allochthonousenergy includesdifferenttypesofplantremains(e.g.leafandflowers frac-tions,wood),animaltissues(carrionandterrestrialinvertebrates), deadmicrobes,extracellularpolymers,rootexudatesandmucilage (Mooreetal.,2004).Inaddition,macroinvertebrateshave consider-ableinfluenceontheprocessingofautochthonousorganicmatter thatcomesfrom theproductionof microalgae,macroalgae and macrophytes(Anderson andSedell, 1979; Vannoteet al.,1980; Minshalletal.,1985;Martínez-Silva,2015).

Many of the physical and biotic variables of rivers show changesalongtheiraltitudinalandlongitudinalgradients(Allan andCastillo,2007).TheoriessuchastheRiverContinuumConcept (Vannoteetal.,1980)emphasizetheimportanceoflongitudinal hydrological connectivity as a key role in thestructure of the communities,becausetheunidirectionalflowofwaterrelatesthe https://doi.org/10.1016/j.rbe.2018.07.003

0085-5626/©2018SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

processes that occurin the downstream sectionsto those that takeplaceupstream.Thus,changesinbioticcompositionandin loading,transport,useandstorageoforganicmatter(OM)along thecontinuumwill berelatively predictable.In temperate lati-tuderivers,forexample,therecurrentseasonaldynamicsmarked bytemperaturevariationshavebeenextensivelystudied(Dallas, 2008;Boyeroetal.,2011;Orretal.,2015;Wagneretal.,2017). Inthoseecosystems,temperatureisanimportantfactor regulat-inginputand transportofallochthonousOM;italsoaffectsthe dispersionoforganismsandinfluencestheavailabilityandquality ofenergysources.Intropicalaquaticsystemsseasonalityis deter-minedmostlybyprecipitation(Boultonetal.,2008;Gonc¸alvesetal., 2014),whichdirectlyaffects thewateramountandquality.The rainyseasonmeansanimportantinputofwaterthatcancondition theamountofOMavailableintheriverbed,andincontrast,thedry periodcanimplyagreaterhydrologicalstability(Brendoncketal., 2015).Changesinwaterflowareconsidereda“mastervariable”in thefunctioningoffluvialsystems,duetoitsinfluenceontheriver’s physical,chemical,and biologicalfeatures(Powersetal.,1995). HydrologicaldynamicsandavailabilityofOMhaveagreatinfluence onthetrophicrelationshipsthatareestablishedbetweenaquatic invertebratesandtheirfoodsources,aspectsthathavenotbeen studiedindetailintropicalrivers(Ramírezetal.,2008;Gonc¸alves etal.,2014).

Studiesoftrophicnetworksareimportantbecausetheyallow ustounderstandtherelationshipsoffooddependence between organismsand,therefore,theconnectionsbetweenbioticelements ofthesystem.Thisinformation canbeveryusefulfor the con-servationandpropermanagementofNeotropicalrivers.Sostrong seasonalityandchangesintemperatureleadtohighlypredictable inputsanddynamicsofOMintemperatestreams.Thiscauses mod-ificationsinthebiologicalassemblagesaccordingtothetemporary changesinOM.InNeotropicalstreamsthermalseasonalityismuch lessmarkedandchangesinOMaredrivenmainlybyhydrology (Gonc¸alvesetal., 2014).Neotropicalrivershave notbeen stud-iedenoughtobeabletoevaluatetrophicnetworksthroughoutthe hydrologicalcycle;however,importantresearchhasbeendoneby MottaandUieda(2005),UiedaandMotta(2007)and Ceneviva-Bastosetal.(2012)insomeBrazilianrivers.Thegoalofthepresent researchwastodescribethestructureofthemacroinvertebrate trophicnetworkthroughananalysisofgutcontentsduringtwo contrastinghydroclimaticperiods(rainyanddryseasons)atthree sitesalonganaltitudinalgradient(60–1700m)oftheGairaRiver(a ColombianNeotropicalriver).Spatialandseasonalvariationsinthe foodwebstructureofthecommunitywereevaluatedtodetermine ifdifferencesinflowandaltitudecausedchangesinthetrophic networkoftheinvertebrates.

AccordingtoVannoteetal.(1980),thequantityandoriginof theOMintheriverchangealongthelongitudinalgradient,then weexpect similarpatternthat wouldaffect thenetwork struc-ture.LowflowsfavorOMaccumulation(Schmid-ArayaandSchmid, 2000)thatcouldbeamoreavailableresourceforinvertebrates.The higheravailabilityinthedryseasoninourrivercoulddetermine somechangesinbasalresourcesandinnetworkproperties. Sea-sonaldifferenceswouldnotbesoobviousinthelowerpartofthe river,wheretheroleofautochthonousOMshouldbegreaterand moreconstantduetothedominanceofFPOM,a productofthe physicalandbiologicalprocessingoftheCPOM.

Materialandmethods

Studysite

TheSierraNevadadeSantaMarta(SNSM)isacoastal moun-tain massif isolated fromthe Andes and characterized by high

biodiversityandendemism.ItislocatedinnorthernColombiaand hastheappearance ofa triangular-based pyramid. Itsnorthern flankbordersoneofthemostaridpartsofthecountry(LaGuajira) andtheCaribbeanSea,theeastflankfacesavalleythatseparates themassiffromtheSerraníadePerijá,thenorthernmost exten-sionoftheAndesEasternCordillera,whilethewesternflankfaces theCaribbeanSea,theCiénagaGrandedeSantaMartaandapart oftheMagdalenaRivervalley.SNSMissubjecttoanthropic dis-turbanceslikedeforestation,theestablishmentofunsuitablecrops oninappropriateanddeficientsoilsandextensivecattleranching. Theseactivitieshaveexertedsignificantpressureonwatersheds causingalterationsinlocalaquaticecosystems.Theimpactofthese activitiesisreflectedinalterationsinthehydrological,physicaland chemicalvariablesoftherivers,suchasincreasedrunoff,flowand temperature,andtheincreaseofnutrientsfromsoilleachinginthe rainyseasons(Prosierra,1998).

TheGairaRiverislocatedonthewesternsideoftheSNSMand hasalengthof32.5kmfromitsheadwatersatthemouthoftheriver whereitemptiesintotheCaribbeanSea.Sampleswerecollectedin threesections,thefirstoneintheupperpart(SanLorenzo)ofthe riverat1700maltitude,thesecondinthemiddlesectionat inter-mediatealtitude(LaVictoria,900m),andthethirdatthelowest part(PuertoMosquito,60m).Attheuppersection,theriparian veg-etationiswell-preservedanddominatedbylargetreesthatprovide shadeovertheriver.Thesite,locatedveryclosetothesourceofthe GairaRiver,issteep(>70◦)withnoanthropicactivities.Inthe mid-dlesection,therearemanycoffeeplantationsandothercropssuch ascornandfruittrees.Thecoffeeplantationsinthemiddlezone canexceed300ha.Theriparianvegetationatthissitecorresponds totreesofconsiderablesize(greaterthan15m)thatofferan exten-sivecanopythatshadestheriversimilarlytotheuppersection.In thelowestsectorshrubvegetationdominateswiththepresenceof sometreesthatprovidelittleshadingovertheriver.Thiszonehas extensiveanthropicinfluenceduetolandholdingsneartheriver thatareusedasspasbytouristsandresidents.Thegeographic coor-dinatesofeachsite,aswellassomeenvironmentalconditionsand physicochemicalwatercharacteristicsarepresentedinTable1.A moredetaileddescriptionofthesesamplingsitescanbefoundin Tamaris-Turizoetal.(2013).

Sampling

Sixintensivesamplingregimenswereconductedateachsite on theGaira River.The whole regionhas a rainy season from ApriltoNovember,and adry seasonfromDecembertoMarch, which in turn causes increases and reductions in river flow (Tamarís-Turizo etal., 2007).Collectionswere doneduring the rainyseasons(October–November2010,2011and2013)anddry seasons(February–March 2010and2011,and December2013). Thesamplescollectedduringthethreeyearsweregroupedby sea-sons,takingintoaccountthecoincidenceinthemonthsofrainfall ordrought.Duringallthesamplings,thefollowingphysicaland chemicalvariablesweremeasuredinsituwithaWTW multiparam-eterportablemeter(Xylem,Germany):watertemperature(◦C),pH (units),conductivity(␮Scm−1)anddissolvedoxygen(mgL−1).In addition,theaverageflowvelocity(ms−1)wasrecordedwitha flowmeter (GlobalWater–FP 211,Xylem,USA).Thedischarge was calculated by multiplying the cross-sectional area by the velocity(ms−1).Simultaneously,watersamplesweretakenfrom theriverwith500mLplasticbottles,thatwerekeptrefrigerated and transferredtotheWater QualityLaboratoryof the Univer-sityofMagdalenatoperformnutrientanalyses(nitrates,nitrites andorthophosphates)accordingtostandardmethodologies(APHA, 1998).Organismswerecollectedinthreetypesofsubstrate:gravel, pebblesandleaflitter.ASurbernet(mesh:250␮m,area:0.09m2_,

Table1

Meanandstandarddeviationoftheenvironmental,physicalandchemicalvariablesinthestudysites.Numberofsamplespersite:6,D,dry;Ll,rainy;ND,nodetermined. Nitrite,nitrateandphosphateinformationwastakenfromRodríguez-Barriosetal.(2011).

Variable SanLorenzo (Upper) LaVictoria (Middle) PuertoMosquito (Lower)

D Ll D Ll D Ll Altitude(m) 1700 900 60 Coordinates N11◦₀₇₃₉ _W74◦₀₃₁₄ _N11◦₀₇_44.2 _W74◦₀₅_35.8 _N11◦₁₀₂₆ _W74◦₁₀₃₇ Averagerainfall(mm) 2683 2249 448 Flowvelocity(ms−1_{) 0.40±0.08 0.73±0.06 0.56±0.45 0.62±0.01 0.21±0.03 0.56±0.10} Discharge(m3_s−1_{) 0.20±0.12 0.39±0.09 0.36±0.17 0.58±0.18 0.36±0.21 0.42±0.02}

Riverchanneldepth(m) 0.20±0.01 0.33±0.03 0.29±0.01 0.42±0.12 0.47±0.50 0.73±0.01 Riverchannelwidth(m) 4.3±0.5 4.8±1.2 5.0±1.2 5.8±1.4 7.14±0.11 12.00±0.31 Watertemperature(◦_{C) 14.10±0.01 15.82±0.02 17.98±0.69 19.10±0.36 24.85±0.39 25.14±0.66} pH 6.68±0.37 7.88±1.16 7.60±0.97 7.02±1.10 7.33±0.16 7.39±0.13 Conductivity(␮Scm−1_{) 39.17±13.76 60.90±3.76 53.29±28.61 76.33±0.52 116.58±14.45 114.83±11.99} Dissolvedoxygen(mgL−1_{) 8.56±0.99 8.70±1.30 7.82±0.73 8.52±0.64 7.14±0.68 8.48±0.54} Nitrates(␮gL−1_{NO3) 0.18±0.09 ND 0.22±0.10 ND 0.24±0.12 ND} Nitrites(␮gL−1NO2) 0.79±0.26 ND 0.79±0.40 ND 1.42±1.11 ND Ortophosphates(␮gL−1PO4) 4.41±2.48 ND 4.77±3.31 ND 4.62±3.16 ND

extractionwasdoneforthepebbleswithdiametersbetween18

and23cminwhichatotalof0.25m2_{ofsubstratawereanalyzed;}

inthelitter500gofwetweightwerecollectedandspecimenswere

extractedmanually.Inallcasestheorganismextractionwasdone

inthefield.Weperformedsamplingtoassuremaximumorganism

representationateachhabitatandthesameeffortinallsites.We

groupedallorganismsateachsubstrateintoanintegratedsample

bysiteandseason.Theinvertebrateswerepreservedin96%ethanol

andtransferredtothelaboratoryforfurtheranalysis.Weidentified

theanimalstothemostdetailedtaxonomiclevelpossibleusing

tax-onomic(genuslevelinmostcases)keyssuchasthoseofWiggins

(1996),Posada-GarcíaandRoldán-Pérez(2003),Domínguezetal. (2006),Merrittetal.(2008),DomínguezandFernández(2009)and Ramírez(2010).

Trophicanalysis

Gutcontents wereanalyzed using a technique proposedby Tomanovaetal.(2006),withsomemodifications.Forthis,the ante-riorpartofthedigestivetractsoffiveindividualsofeachtaxon wereextracted;taxarepresentedbylessthanfiveindividualswere analyzedindividually.Whenanalyzedthefivegutcontentswere combinedandhomogenizedwithglycerinonamicroscopeslide. Wetookphotomicrographsof20randomfieldswithanAxioCam ERc5scamerafittedtoaCARLZEISSPrimoStarmicroscope(Zeiss, Germany)using10×and40×magnification.Whenthegutshad lit-tlecontent,theentiresheetwasphotographed.Fromtheseimages, thepercentage ofeach fooditem in thestomachcontents was identifiedandquantified.Thefoodcategorieswereanimaltissue (AT,insectswere identifiedtogenus wheneverpossible);plant tissue (PT);microalgae(MI)and fungi(FUN) whosecells could beidentifiedundermicroscope;coarseparticulateorganicmatter >1mm(CPOM,amorphousmaterialthatcouldnotbeidentified undermicroscope); and fine particulate organicmatter (FPOM, organicparticlesbetween50␮mand1mm).Inordertoconfirm therelationsofconsumptionandtoassignatrophiccategorytothe organisms,wereferredtothestudiesofMottaandUieda(2004), Tomanovaetal.(2006),Charáetal.(2012)andReynagaand Rueda-Martín(2014).

Dataanalysis

Weanalyzedconsumerrelationsusingabinarymatrixof preda-tor vs. prey. This matrix was based on an analysis of the gut contents and these data were used to visualize the models of trophicnetworks.Ateachsiteandseasonweestimatedthe fol-lowingattributesofthetrophicnetworksaccordingtoDunneetal.

(2002):thenumberoftrophicspeciesorthenumberoftaxa(S); thenumberoflinks(L,eachpairwiseinteractionsinthenetwork, establishingthepredator-preyinteractionsthroughthe identifi-cationatthegenusleveloftheorganismsinthegutcontents); thelinkdensity(L/S,averagenumberoffeedinglinksperspecies); andtheconnectance(C=L/S2_{,theproportionofpossiblelinksthat}

occurbetweenspecies).Standarddeviationsofbothgenerality (SD-G)andvulnerability(SD-V)werethenormalizedmeannumberof preyperconsumerandthenormalizedmeannumberofconsumers perprey,respectively(Bersieretal.,2002),thus,SD-Vofanodeis thenumberofspeciesthatisconsumed,normalizedbyL/S.Other variablesthatwerecalculatedfromthetrophicnetworkweremean chainlength(mCL),maximumchainlength(maxCL)andfractions ofbasalresources(b)intermediatetaxa(i)andtoptaxa(t)(topif thetaxonhaspreybutnoconsumers,intermediateifithasprey andconsumers,andbasalifitonlyhasconsumers,Bersieretal., 2002).Alltrophicanalysesandtrophicmodelswereperformedin theNetwork3Dprogram(Yoonetal.,2004;Williams,2010).A dis-criminantanalysiswascarriedoutusingthemeanvaluesofgut contentareatoevaluatethevariationinthecompositionofthe foodresourcesconsumedatthedifferentsitesandseasons.This analysiswasperformedwiththeRWizard2.3program(Guisande etal.,2016).

Results

Atotalof698gutsbelongingto48taxaofaquatic macroinverte-bratesweredissected.Atallsitesthetrophicspeciesrichnesswas higherduringthedryseasons(from31to33species).Thehighest numberoftrophicspecieswasfoundintheupperpartduring peri-odsofdrought(33).Atthissamesite,thelowestnumberoftrophic specieswasfoundduringtherainyseasons(17).Thecomposition ofthecommunitieswassimilarbetweentheclimaticperiods (Sup-plement1).Whencomparingsites,thelowestsectionshowedthe lowestvalueandtheuppersectionshowedthehighestvalue.The numberoftrophiclevelsandthemaximumfoodchainlengthwere similarbetweensites(aboutthreeinallcases)(Fig.1andTable2). Theproportionsoftoptaxa(t)showedanimportantseasonal vari-ationinthehighestsectionoftheriverfrom0.58duringthedry seasonsto0.29duringtherainyseasons.However,themiddleand lowersectionsshowedvaluesof0.53and0.58duringthedry peri-odsand0.41and0.29duringtherainyphasesrespectively.The oppositeoccurredwiththefractionoftheintermediatetaxa(i)on thelowestsection,whichwasreducedduringthedryseasons com-paredtotherainyseasons.Fractionsofbasalspecies(b)werelowat allsitesduringthedryseasonswithslightlyhigherrecordsduring therainyseasons.Connectance(C)waslowatallsitesandduring

SL - D LV - D PM - D PM - R LV - R SL - R PT PT PT PT MI MI PT COPM COPM COPM COPM COPM COPM MI PT FUN FUN FUN FUN FUN FUN MI MI MI FOPM FOPM FOPM FOPM FOPM FOPM

Fig.1.StaticmodelsoftrophicnetworksatthreesitesintheGairaRiverrepresentingbasalresources(red),intermediateconsumer(orange)andtoppredators(yellow)and theinteractionsamongthem.SL,SanLorenzo,uppersector;LV,LaVictoria,middlesector;PM,PuertoMosquito,lowersector;D,dryseason;R,rainyseason.

Table2

Attributesofthemodelsoftrophicnetworksatthethreestudysites.SD,standarddeviation;Fr,fraction.

Site SanLorenzo (Upper) LaVictoria (Middle) PuertoMosquito (Lower)

Dry Wet Dry Wet Dry Wet

Trophicspeciesrichness(S) 31 17 32 24 33 22

Numberoftrophiclevel 2.87 2.83 3.12 3.10 2.87 3.12

Numberoftrophiclinks(L) 77 39 87 75 123 42

Linkagedensity(L/S) 2.48 1.77 2.71 3.12 4.33 2.47

Connectance(C) 0.08 0.08 0.08 0.13 0.13 0.14

SDgenerality(SD-G) 1.15 0.93 0.82 0.84 0.60 1.13

SDvulnerability(SD-V) 1.90 2.13 1.99 1.49 1.87 0.98

Meanchainlength(mFCL) 1.95 1.81 1.93 1.92 2.03 1.84

Maxchainlength(maxFCL) 3.00 2.83 3.13 3.10 3.00 3.12

Fr.Numberofbasaltaxa(b) 0.15 0.23 0.16 0.21 0.15 0.29

Fr.Numberofintermediatetaxa(i) 0.27 0.23 0.31 0.37 0.27 0.41

Fr.Numberoftoptaxa(t) 0.58 0.54 0.53 0.41 0.58 0.29

thetwosetsofclimaticperiods,althoughitwasslightlyhigherin

theuppersectionoftheriver(Table2).

Inthehighestsection,thestandarddeviationofthegeneralists (SD-G)duringtherainymonthsalmostdoubledfromthatofthedry seasons.Thestandarddeviationofvulnerability(SD-V)waslower intherainyseasonsinthemiddleanduppersectionsoftheriverbut increasedastheelevationincreased(Table2).TheSD-Vvaluesof themainfoodresourcesincreaseddownstream(Fig.2).Theseitems wereCPOM,FPOMandplanttissues,whichconstitutesthebasal sourceswiththehighestproportioninthegutsoftheconsumers inthethreetrophicnetworks.TheFPOMwasthemostimportant itematthethreesites,butitsSD-Vvaluesdecreaseddownstream, independentlyofthehydrologicalperiod.Duringthedryseasons theCPOMhadaninversebehavior,withtheSD-Vincreasingatthe lowestsite,whereasduringtherainyseasonitwasslightlyhigher inthemiddlesectionsoftheriver.Theplanttissuesshowedlittle

altitudinalvariationinthedryseasonsandclearlyincreasedinits SD-Vvaluesastheelevationincreasedintherainyseason.Results showedthegreatimportanceofFPOMalongthealtitudinal gradi-entinthistropicalriver,especiallyattheupperandmiddleparts oftheriver,evengreaterthanthatofCPOMandplanttissues.The FPOMwasthemostcommonfooditemforconsumersinall sec-tions.Inthemostelevatedpartoftheriver,althoughtheFPOM showedthehighestSD-V,itsvaluedecreasedduringtherainy sea-sons.InthemiddlesectionFPOMandCPOMwereimportantitems, particularlyduringthedryseasons.DuringthedryseasonstheSD-V oftheCPOMwasnotableinthelowestsectionoftheriver(Fig.2). Asobservedinthediscriminantanalysis(Fig.3),duringdry peri-odsFPOM,CPOM,animaltissuesandplanttissueswerethemost consumedresourcesinupperandmiddlesections.In thelower parts,animportantcontributionoftheFPOM,microalgaeandfungi wereobserved.Thelasttwofooditemscontributedtothedefinition

FPOM CPOM PT FPOM CPOM PT 9.66 9.59 9.56 4.38 2.82 3.62 5.76 3.67 4.02 3.68 4.61 4.41 6.46 2.88 0.22 3.95 2.88 1.62

Fig.2. Representationofthestandarddeviationofvulnerability(SD-V)ofthemainfoodsources(FPOM,fineparticulateorganicmatter;CPOM,coarseparticulateorganic matter;PT,planttissue)calculatedfromtheratiosrecordedinthegutsofthemacroinvertebratessampledintheelevationalgradientofGairaRiverduringthedryandrainy seasons.Arrowthicknessindicatesthevulnerabilityimportance.

Dry season Rainy season 2 0 -2 -4 -6 -1 0 2 1 3 -2 -3 -4 -3 -2 -1 0 -4 -2 0 2 1 PT FPOM CPOM AT MI FUN San lorenzo La victoria Puerto mosquito CAN 2 9.05% CAN 2 31.89% CAN 1 90.95% CAN 1 68.11% FPOM FUN PT CPOM AT MI

Fig.3.Discriminantanalysisofpercentagesofgutcontentsformacroinvertebratesanalyzedatthethreesamplingsites.FPOM,fineparticulateorganicmatter;CPOM,coarse particulateorganicmatter;FUN,fungi;AT,animaltissue;PT,planttissue;MI,microalgae.

ofthegroupsseenonthemiddleandlowestreachesoftheriver. Incontrast,duringtherainyseasonstheconsumptionofresources wasmoreheterogeneousateachofthethreesites.Thefractions ofCPOMandFPOMwereelevatedinmiddleandlowestsections, whereasfungishowedhighercontributionsontheuppermostand middlepartsoftheriver(Fig.3)andthiswasnotseenduringthe dryseasons.

Discussion

Our assumption of a higher accumulation of CPOM during dryperiod wasnotpossibletoverify,because,it wasthemost importantresourceduringdryandwetseasons.AlthoughCPOM contributioninthefoodwebwashigherduringthedryseasons, thisonlyoccurredinthemiddleandlowestsectionsoftheriver. ThereseemstobelessretentionofCPOMduringtherainyseasons (Rodríguez-Barriosetal.,2011)and,therefore,thereisatendency foralowercontributionofthisitemtothefoodchainsasexpected butthisoccurredmainlyinthelowestriversection.Duringthedry periods,thelowestriverflowsincreaseretentionoforganicmatter suchasleavesandsmallfragmentsofwood.Thisisbecausethe lowflowsarenotcapableofsuspendingthebottommaterialand moveitwiththerivercurrent(Rollsetal.,2012).Consideringthe contributionofFPOMduringthedryseasons,highervaluesof SD-Vwereconfirmedforthisperiodofgreaterwaterstabilitywhen comparedtotherainyseasons(Cheshireetal.,2005;Boultonetal., 2008).However,unlikewhatwasexpected,inthelowestsection oftheriverthereweremarkedseasonaldifferencesinthetwoOM fractionsandinthevegetaltissuescontainedinthestomachsof theinvertebrates.

Resultsindicatethatthetrophicnetworksvariedbetweenthe twoseasons.Duringthedryseasonsthefoodwebattributeswere similaratallsites,afactthatisrelatedtothestabilityofthe sys-temandanincreaseintheretentionoftheCPOM.Duringtherainy seasonsthefoodwebshadlowernumbersoftrophicspeciesand linkdensity,butmorebasalspeciesthatcouldbeassociatedwitha lowercontributionofCPOMtothetrophicnetworkandingeneral withasmalleramountofresourcesthroughafoodwebthathas alowerdensityoforganismsinthesewetperiods.Althoughwe expectedgreatcontrastsalongthealtitudinalgradient,the differ-encesintheattributesofthenetworkswerenotverydrastic.This maybeduetosomeaspectsoftheriver’sgeomorphology,suchas theshortlengthofthemainchannelandthestrongslopesofthe riverbasin(WebsterandMeyer,1997;Prosierra,1998).

Thenumberoftopspecies,theincreaseofbasalspecies,andthe connectanceshowedvariations,especiallyinthealtitudinal gra-dient.Thiscoincideswithotherresearchdoneintropicalstreams ofAustraliaandVenezuela(Cheshireetal.,2005;Laymanetal., 2005).However,inourstudythevaluesofthesetrophicnetwork propertieswerelower,whichmightbeduetothetaxonomic reso-lutionusedinourwork(Supplement1).Specificallyforthecaseof planttissueandmicroalgae,itispossiblethatthenumberofbasal speciesisundervalued,becausetheseitemscouldonlybe catego-rizedbylargegroups,withoutbeingabletoarriveatmoreprecise taxonomicdetail.Theincreaseinthefractionofbasalspeciesand thecorrespondingreductioninthefractionofintermediatespecies observedduringtherainyseasonsatallsitesarerelated tothe disturbanceeffectgenerated bytherunoffduringtheseperiods (Cheshireetal.,2005;MottaandUieda,2005;Pedroza-Ramosetal., 2016).Further,theincreaseoftopspeciesduringthedryseasons couldbeassociatedwith(1)thegreaterstabilityoftheriver cur-rentandconsequentlytoagenerallylessvariablesystemand(2) withthecapacityoforganismssuchasthePlecopteraand Mega-lopteratoattachthemselvestosubstrateswheretheylive.InBrazil, Krawczyketal.(2013)alsofoundahighernumberofpredators

dur-ingthedryseasonandthisresultmightberelatedtothereduced volumeofwaterfavoringthecolonizationofmanypreytaxaalong theriversothattopspecieshaveagreaternumberofresources. Itispossiblethatamorerestrictedwetzoneconstrainsaquatic organismstoasmallersurfacearea,whichwouldfavorpredators (describedfortemporaryriversduringthedryphase)(Gasithand Resh,1999).

Thealtitudinalgradientaffectedtosomeextentthenumberof linksinthetrophicnetwork,sincethisattributeincreasedwitha decreaseintheelevation,butthiswasnotevidentinother charac-teristicsofthetrophicnetwork.Itispossiblethatthelowestsector ofthisriverhasthehighheterogeneityofmicrohabitats( Tamaris-Turizoetal.,2013),duetothedecreasedslopethatdoesnotfavor thecreationofdifferentsubstrata,which inturngenerateslow speciesdiversity,speciallyduringrainyseason(Ceneviva-Bastos etal.,2012).Also,humanimpactsintheregionarelikelyto con-tributetofewerlinksinthelowestsectionoftheriver.Ineffect,the altitudinalgradientalsocorrespondstoanimpactgradient.Other researchhasshownthatthepropertiesoftrophicnetworksvary withelevation;Romanuketal.(2006)havedocumentedthe vari-ationinthestructureofthetrophicnetworkintemperaterivers ofCanada.Theseauthorscomparedthenetworksinthreerivers along analtitudinal gradient(mountainouszone,piedmontand plains)andfoundthatthepercentageofintermediatespeciesand thepercentageofherbivorywerehigherinthemiddlesections, whileconnectanceandcannibalismhadthegreatestimpactonthe uppersections.

Maximumfoodchainlengthwasnotaffectedbyaltitudinalor seasonalchanges.Itremainedthesameinboth typesof hydro-logicalperiodsandhadsimilarmagnitudestothoserecordedin othertropicalrivers(Laymanetal.,2005;MottaandUieda,2005). Thedecreaseinthenumberoflinkscausedagreaterconnectance upstream,butmainlyduringtherainyseason,probablyduetoa decreaseintheaveragespeciesrichnessofthetrophicnetwork. However,theseanalyseswerebasedonlyonmacroinvertebrate communitiesanddidnotincludegroupssuchasfishand amphib-ians,whichareveryimportantinthetransferofenergyinthese systems (Ranvestel et al., 2004; Barros-Maestre and Granados-Martínez,2016).We,therefore,expectedthatthefoodchainlength intheGairaRiverwouldbelongerifthesehigherconsumersare takenintoaccount.

Thetrophicnetworksdrawnwiththeresultsofthegut con-tentanalysishighlights theimportanceofFPOMasafooditem that dominates mostaquaticinvertebrates (Covich et al.,1999; Mooreetal.,2004;Amadeu-Santana etal.,2015;Ferreiraetal., 2015).Thisfactwasevidentinthepresentstudybecauseitwas theresourcewithgreatervulnerability(SD-V)duringthetwo sea-sonsattheupperandmiddlesites.However,stableisotopeanalysis is required tocheck for the extent towhich FPOM is actually assimilated.Otherwise,CPOMseemedtobeanimportantresource, especiallyduringthedryseason,whentheretentionofleavesis high(Rodríguez-Barriosetal.,2011)andthemacroinvertebrates areconcentratingbecauseofthereductioninflow.Onthemiddle partoftheGairaRiver,where65%ofplantmatterbelongstoleaves fromtheriparianforest(Collantesetal.,2014),theprocessingof litterfallincreasedduringthedryseason.

Theobserveddifferencesintheconformationofthefoodweb inthediscriminantanalysesduringwetanddryseasonsalso con-firmsthechangesinthesupplyandavailabilityofresourcesinthe river.Duringthedryseasonthesystemismorestable,whichmight allowtheCPOMtoberetainedbytherocksandthetrunksthatare inthechannel.Therainyseasonsfavorthetrawlingofnutrients fromtheriverside(Ramírezetal.,2007),afactthatseemsto stim-ulatethegrowthoffungiandmicroalgaeondifferentsubstrates (leaves,logs,rocks),especiallyinthemiddleandlowestsections. TheloweravailabilityofCPOMduringtherainyseasonsforcedthe

invertebratestofeedonalternativeresources,asobservedwiththe greaterabundanceofalgaeinthegutcontents.Asexpected,inthe lowersectionsoftheGairaRivertherewillbeagreatertendencyfor autochthonousorganicmattertocontributetothetrophicnetwork oftheinvertebratecommunity,ashasbeenreportedforaBrazilian river(Neres-Limaetal.,2016).

Insummary,thevariabilityofthehighandlowwaterperiods intherivercausedremarkableseasonalchangesinthestructureof thefoodwebintheGairaRiver.Changesinthefoodwebattributes weremorerelevantcontrastingbothseasonsthancontrastingthe longitudinalgradient.Fineandcoarseorganicmatterarethemost abundantresourcesintheguts oftheinvertebrates,which isin accordancewithmostofthefluvialfoodwebsaroundtheworld. However,inthisNeotropicalrivertheavailabilityoftheorganic matter,andconsequentlythefoodwebstructure,weremore deter-minedby seasonalchanges inhydrologythan byalongitudinal continuum.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

ThankstoMaríadelCarmenZú ˜niga,NarcisPrat,PabloGutiérrez, CarlosMolineriandEduardoDomínguezfortheircollaborationin theidentificationofanimaltissues,tothemembersoftheResearch GrouponAppliedBiodiversity(GIBEA)forthesupportinfieldtrips, andtoCOLCIENCIAS(scholarshipgrantedtoC.E.T.T.incall6172). AdditionalthanksgototheUniversityof Magdalenafor logisti-calandeconomicsupport,totheOfficeoftheVicePresidentfor Research ofthe NationalUniversity of Colombiafor thepartial financingoftheproject(code:34582)andtotheConsejo Profe-sionaldeBiología(CPB)fortheeconomiccontributionthrougha researchgrant(2016).

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,atdoi:10.1016/j.rbe.2018.07.003.

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