The ecological footprint of Acca sellowiana domestication maintains the residual vertebrate

24 Pages·2017·16.77 MB·English

RESEARCHARTICLE
The ecological footprint of Acca sellowiana
domestication maintains the residual
vertebrate diversity in threatened highlands
of Atlantic Forest
JulianoAndre´Bogoni1☯*,Maur´ıcioEduardoGraipel2☯,NivaldoPeroni1☯
1 ProgramadePo´s-Graduac¸ãoemEcologia,DepartamentodeEcologiaeZoologia,UniversidadeFederal
deSantaCatarina,Floriano´polis,SantaCatarina,Brazil,2 DepartamentodeEcologiaeZoologia,
UniversidadeFederaldeSantaCatarina,Floriano´polis,SantaCatarina,Brazil
a1111111111 ☯Theseauthorscontributedequallytothiswork.
a1111111111 *[email protected]
a1111111111
a1111111111
a1111111111 Abstract
Pastandcontemporaryhumanactionsarecausingnumerouschangesinpatternsandpro-
cessesatvariousecosystemscalesandtrophiclevels,includingunintendeddownstream
changes,suchasspeciesinteractions.InitsnativerangeAccasellowiana(Feijoa)com-
OPENACCESS
binessomecharacteristicsofhumaninteractions:incipientdomestication,restrictedto
Citation:BogoniJA,GraipelME,PeroniN(2018)
subtropicalAtlanticForesthighlands,associatedwiththethreatenedconiferAraucaria
TheecologicalfootprintofAccasellowiana
angustifolia(Araucaria),withinadomesticatedlandscapewithanthropogenicforest
domesticationmaintainstheresidualvertebrate
diversityinthreatenedhighlandsofAtlanticForest. patches,andprovidesfruitatatimeofresourceshortage(Araucariaseeds—pinhão).We
PLoSONE13(4):e0195199.https://doi.org/ quantifythetrophicrelationshipsbetweenFeijoaandvertebrates,andevaluatetheinflu-
10.1371/journal.pone.0195199
encesoninteractionscausedbyenvironmentalvariations,Feijoadomesticationevidences,
Editor:ManuESaunders,UniversityofNew spatialdistanceandfruitavailability.Infoursiteswithinprotectedareas,weselected28
England,AUSTRALIA
focalindividualsofFeijoa(seven/site)andcollectedthreetemporalreplicasbetween2015
Received:July9,2017 and2016,whenwemeasuredproductivityandfrugivoryvia45-secondvideostakenwith
Accepted:March13,2018 cameratraps.Usingecologicalnetwork,rarefactioncurvesandvariationpartitioninganaly-
ses,weevaluatethefrugivorynetworktopology,thespatiotemporalstructureofcommuni-
Published:April4,2018
tiesinrelationtofruitavailabilityandtheinfluenceofpredictivevariablesonfrugivory.We
Copyright:Thisisanopenaccessarticle,freeofall
foundalargespatiotemporalvariationinproductivityofFeijoaandthat20speciescon-
copyright,andmaybefreelyreproduced,
distributed,transmitted,modified,builtupon,or sumedFeijoafruits,withaspeciesdegreeof2.8(±5.7)andaverageFeijoadegreeof14.4
otherwiseusedbyanyoneforanylawfulpurpose. (±10.1),inamodularnetworkwithintermediaryconnectance.Rarefactioncurvesshowed
TheworkismadeavailableundertheCreative
thatrichnessandtheindependentrecordsarecongruentwiththefruitamount.Variation
CommonsCC0publicdomaindedication.
partitioningshowedthat,forthefocalindividuals,canopyarea,greencoverage,patchsize
DataAvailabilityStatement:Allrelevantdataare
anddistancetowaterinfluencedfrugivory,andtheFeijoadomesticationinfluencedsignifi-
withinthepaperanditsSupportingInformation
files. cantlythemammalianfrugivory.Feijoaisanimportantresourcethatprovidesfoodduring
thetimeofyearwhenPinhãoisabsent,andattractsfrugivores,maintaintheresidualdiver-
Funding:ThisworkwassupportedbytheBrazilian
MinistryofEducation(CAPES),Ph.D.scholarship sityofvertebratescontributingtothestructureofcommunitiesinhighlands.Ourinsights
(JAB)and(CNPq)productivityfellowship(NP). allowedustoevaluatethemagnitudeoftheinteractionsbetweenvertebratesandanincipi-
Competinginterests:Theauthorshavedeclared entdomesticatedtree,inaculturallandscapeandhighlythreatenedenvironment,undera
thatnocompetinginterestsexist.
PLOSONE|https://doi.org/10.1371/journal.pone.0195199 April4,2018 1/24
Feijoadomesticationmaintainstheresidualvertebratediversity
basalfoodwebapproachwithimplicationsforbottom-upandtop-downforces.Theresults
contributetounderstandinganimal-plantrelationships,includingconceptsthatcanberepli-
catedforothersessilepreyandmobilepredatorsinanyregionorhabitatunderdifferentgra-
dientsofmanagement.Thus,thisworkshowshowhumanactionscanchangenotonly
patternsofdistributionandabundancebutalsothediversityanddirectionofinterspecific
interactionsamongspecies.
Introduction
Ecologicalsystemsarecomplex,dynamic,self-organized,withemergentproperties,andfeed-
backs[1].Inaddition,pastchangesandthepersistentfeedbacksgeneratedbyhumanecosys-
temengineersincoconstructedlandscapeswithnaturehaveimportantimplicationsfor
currentdiversitypatternsandecologicalprocesses[2–3].Yet,contemporaneousdisruptions
canpromotenumerouschangesandmoveecosystemsfromonestablestatetoanotherstable
alternative:aprocessknownasphaseshifts[4].Oneofthesedisordersis“Anthropocene
Defaunation”:aprocessofextinctioncausedbyhumanimpacts[5–6].Themainhuman-
drivencausesofdefaunationandcompositionalchangesarehabitatloss,fragmentation,hunt-
ingandforestconversion[7–8].Compositionalchangesandselectivespecieslossincommu-
nitiescanproducestrongside-effectimpactsonecosystemfunction,promotingcascade
effectsatseveralscales[9].Theseeffectsincludeevolutionarychanges(e.g.,decreasingseed
size)andaffectpopulationdynamicsandcommunitystructure(e.g.,changesinthedetritivore
foodweb,seeddispersalandtrophicwebs,andrearrangementsoftop-downandbottom-up
forces)[9–11].
Thetop-downmodelofcommunityregulationpredictsthatorganismscanbelimiting
resources,bothaspredatororprey,dependingontheirpositioninthefoodweb[12].The
effectivenessoftop-downvs.bottom-upforcesinthechaindependsinpartonhowmanyeffi-
cientconsumersexploittheirprey[12].Thechaindynamicmodelsoffoodwebsareoften
unpredictablebecausedifferentassumptionsaboutmechanisms(e.g.,co-limitationbypreda-
torsandresources)leadtodifferentpredictions(e.g.,consumerefficiencyatamulti-trophic
level)[13].Amongvariousprocessesthatfitthesepremises,frugivoryisanidealcandidatefor
theseecologicalandevolutionaryanalyses[14–16].Patternsandprocessesofpredation/dis-
persalofseedsarehighlystructuredandcoevolvedspatiotemporally[14],withpotentialalter-
ationspromotedbothbypasthumandrivers[2]andcurrentdisturbances[9].Plant-animal
interactionswithinacommunityshouldconsidertheenergyusedattheindividuallevel[14,
17].
Mammalsandbirdsdisperseabout90%ofthewoodyplantspeciesthatproducefruitsin
Neotropicalenvironments,generatinganimportantfeedbacktoplantfitnessandforestregen-
eration[15,18].IntheAtlanticForestofSouthAmerica,thefamilyMyrtaceaeisanimportant
groupofwoodyspeciesandresourceproviderforarangeofvertebratetaxa[19–20].Myrta-
ceaespeciesarethemaincomponentsofloweraltituderainforests,wheretherecanbeover
50speciesinarelativelysmallspace(~1ha)[21–22].InsubtropicalAtlanticForest,Myrtaceae
ingeneralarecloselyassociatedwiththethreatenedconiferAraucariaangustifolia(Araucaria),
whichformOmbrophilousMixedForest(FOM)[23].ForestsdominatedbyAraucarias
havebeenusedasaproxyforconservationstrategies[24].WithinFOMthereisavegetation
mosaicofhighlands(e.g.,uppermontaneforest,swamps,andnativegrassland)thatisspatially
restrictedandhighlyendangeredmainlyduetoclimatechange[24–26].Ininterspersedforest
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Feijoadomesticationmaintainstheresidualvertebratediversity
patchesinthismosaic,Araucariasdominatetheupperstratum,whileMyrtaceaeandLaura-
ceaearethemainfamiliesthatformthemiddleandlowerstrata[27–28].
AfewMyrtaceaespeciesdominatetheflorainhighlands,whichareusuallycharacterized
bysmallfruits(<1cmofdiameter)[29–30].AnexceptiontothisisAccasellowiana(Berg)
Burret(Feijoa).FeijoaisatreenativetoSouthernBrazilandnorthernUruguaythatis
restrictedtoareasinSouthernBrazilover800metersabovesealevel(m.a.s.l.)associatedwith
FOM[23,31].Feijoaispollinatedbybirdsandbees[32–33],andproduceslargefruits(20to
250g)withsmallseeds(~3mm)[29].LikeAraucariainlocallandscapes,Feijoahasbeensub-
jectedtohistoricalanthropogenicinfluencepromotingacertainlevelofdomesticationof
somepopulationsinsitu,whichhasresultedinincreasedfruitsizeandproductivitybyhuman
selection[23,34–36].Currently,withinFOM,Feijoaisusedinseveralways(circa14)bylocal
peoplethatmanagethespeciesviapruning,transplanting,propagationbyseedsandvegetative
propagation[23].Itsdomesticationisincipient[23],aprocessthatexhibitsphenotypicvaria-
tionwithintherangenormallyfoundinwildpopulations[37–39].Moreover,theexpansionof
FOMbypre-Columbianpeople(i.e.,indigenousXoklengandKaingang)favoredtheexpan-
sionofFeijoaandotherassociatedMyrtaceae[23,35].Inaddition,thepastandcontempora-
neousmanagementofFeijoaandAraucariaincreasedtheavailabilityofresourcesinFOM
[23,35].
Plantandanimaldomesticationisthemostimportantdevelopmentofhumanhistorysince
13,000yearsago,andchangedthecourseofhumanity[40].SinceDarwin(1859),domesticated
systemshaveplayedacriticalroleinthedevelopmentandtestingofevolutionarytheory[41].
Managementofnativefruitsinsitu,bothbyindigenouspopulationsandlocalfarmers,isa
recognizedconservationpracticethatcontributestogeneticdiversityandseveralecological
processesthroughdownstreampropagationwithinbiologicalnetworks[42–45].Anotherout-
standingcharacteristicoflocallandscapedomestication—humaninterventionintheland-
scapecomponentsresultinginchangesinevolution,ecology,interactionsandspecies
demography[3,37]—isthepresenceofBostaurus(cattle)anditsimpacts[36].Cattleisan
allochthoneelementthathasbeenmanagedforalongtime(>100years)bylocalsmall-scale
landownersinhighlandsofsubtropicalAtlanticForest[36].Understandingthecomplexeco-
logicallegacyofmanagementinpastlandscapesandtheirusecomponentsisimportantwhen
debatesareragingaboutthefutureofforestsinrelationtonewhumancolonizationdynamics,
climatechange,contemporaneouspoliticalconflictanddefaunation[2,46].
Currently,primarydispersionofFeijoaisbarochoric[47],becausethedistributionregion
ofFeijoaoverlapareasunderaconstantdefaunationoflarge-bodiedvertebrates[8],remaining
onlyaresidualdiversityreducedtoapaleshadowoftheonceamazingbiotaoftheAtlantic
Forest.Yet,Feijoastillhasaposthocassociationwithfrugivores[29].Thefunctionallossof
largefruit-eatingvertebratescandecreaseFeijoafitnessnearconspecificadults[16,48],dis-
ruptsthenaturalregenerationdynamicsofplants,andchangesthemaincomponentsofthe
dispersalprocess[16,49].ThereislittleempiricalinformationontheinteractionofFeijoa
withitsassociatedfauna,althoughtheremaybemanyspeciesthatfeedonitsfruits,asfound
forotherMyrtaceaespecies,resultinginfeedbackthathelpsmaintainecosystemprocesses
[13].
Therefore,asatemporaryalternativeduringtheaustralsummer-autumnwithscarce
resources(mainlytheabsenceofpinhão),Feijoacanactasanattractor,contributingtothe
structureofanimalcommunitiesandcanmaintaintheresidualdiversityofvertebratesin
SouthernBrazilhighlands.Theaimofthisstudywastoprovideascenarioofthetrophicrela-
tionsbetweenFeijoa(aspeciesunderincipientdomesticationandanalternativeresourcein
threatenedhighlands)andlocalwildlife(whichhasexperienceddefaunationeffectsinaland-
scapeinfluencedbyhistoricalmanagement),toevaluatethespace-timecongruencebetween
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Feijoadomesticationmaintainstheresidualvertebratediversity
diversitypatternsandresourceproductivity.Additionally,weaimedtoevaluatetheinfluence
oftheenvironment,thespatialdistanceamongsites,theFeijoadomesticationevidence,and
theresourceofferontheintensityoffrugivory.Weposedthreehypotheses:(1)mammalsand
birdsthatremovefruitsofAccasellowiana–assumingaprioridefaunatedsites—aresmall-to
medium-bodiedfrugivores-herbivore-omnivoresandthecattle;(2)theseasonalFeijoafruit
structuresthevertebratefaunainspaceandtime,increasingthediversitypatternsincongru-
encewithfruitoffer.Theproductivityislinkedwiththeincipientdomesticationprocess,and
thepositiveeffectoffruitofferincludespeciesthatdonoteatfruits,animplicationofbottom-
upcontrolwithhistoricalinfluences;and(3)thenumberofinteractionsarerelatedtoenviron-
mentalpatterns,spatialdistances,Feijoadomesticationevidenceandresourceproductivity.
Boththisfactorsdirectlyorindirectlyreflectslocallandscapedomesticationasawhole.
Materialandmethods
Ethicsstatement
Datacollectionwasauthorizedbasedonlicensenumber47255fromInstitutoChicoMendes
deConservac¸ãodaBiodiversidade(ICMBio).Withinprivateland(ReservaParticulardoPatri-
moˆnioNatural(RPPNs))weconfirmthattheownerofthelandgavepermissiontoconduct
thestudyonthissite.Weconfirmthatthefieldstudiesdidnotinvolvemanipulationofendan-
geredorprotectedspecies,onlyspeciesrecordsviacamera-trap.Vertebraterecordswereper-
formedwithnon-invasivesampling(i.e.camera-trap).Theworkwasnotsubmittedtoan
InstitutionalAnimalCareandUseCommittee(IACUC)orequivalentanimalethicscommit-
tee,becausethedatawerecollectedonlywithcamera-trap.Samplingproceduresand/orexper-
imentalmanipulationswerereviewedorspecificallyapprovedaspartofobtainingthefield
permitbythelicensenumber47255fromInstitutoChicoMendesdeConservac¸ãodaBiodi-
versidade(ICMBio).
Researchareasanddesign
WeselectedfoursitesinprotectedareasofsubtropicalAtlanticForesthighlands,insouthern
Brazil:withinSãoJoaquimNationalPark(S1andS2),surroundingsofRPPNGrandeFloresta
dasArauca´rias(S3),andwithinRPPNLeãodaMontanha(S4)(Fig1;S1Table).Allareasfall
withinthehumidsubtropics(Cfa:Ko¨ppen-Geigerclassification)[50],andareunequalinage
andtermsofprotection,butsharesimilaritiesinmanagementandhistoricalexploitation[36,
51].Sitesliewithinaradiusofcirca40kmand—basedonpreviousstudiesandunpublished
data—hasasimilarcompositionandrichnessoffauna,includingdefaunationindexes,and
presumablyasimilarbiotaatpre-Columbianera[6;Bogonietal.unpublisheddata].Theareas
featureelementsofculturallandscapes,whichincludeanthropogenicforestswithdifferent
intensitiesofpastandpresentuse[35–36]andregenerationstages,formedbyAraucariaForest
(FOM),cloudforest,andnativegrassland[52].Theseareasrepresentamosaicofforest
patchesandhigh-altitudegrasslandcomposedbyoldruralproprietiesdestinedforcattle
breeding,loggingandPinhãoextraction.Theseoldproprietieswereabandonedformorethan
10years,andarecharacterizedforthepresenceofrockstructurestoretainthecattle(taipas),
thefoundationofold-houses(taperas),andotherstructureslinkedtopastlivestockactivities.
AnexceptionisinS3thatremainwithintensivelivestockactivity.Moreover,inthesitesS1,S2
andS4havethepresenceofFeijoatreestypicallymaintainedwithmanagement(e.g.,tracesof
pruning,producinglargestfruitsandlocatedneartooldproprietiesfoundations)[23,37].
Thesechangesinspeciestraitsstartingfromwildancestors(e.g.,changesonthemorphology
ofaerialvegetativepartsandselectionoffruitssizeandquality)areclassicalsyndromesof
domesticationinfoodcrops[53].
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Feijoadomesticationmaintainstheresidualvertebratediversity
Fig1.Researchareas(politicalsizedotted),sitesandsampledesigntoevaluatetheremovalofAccasellowianafruit
byvertebratefauna(mammalsandbirds)inhighlandsofsubtropicalAtlanticForest,Brazil.Inblack:polygonofthe
site(basedonlowlandareaorfragmentsize);ingray:theremnantofAtlanticForestinyears2008–2010;linesinblack:
rivers.S1andS2:SãoJoaquimNationalPark;S3:surroundingofRPPNGrandeFlorestadasArauca´rias;andS4:RPPN
LeãodaMontanha.
https://doi.org/10.1371/journal.pone.0195199.g001
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Feijoadomesticationmaintainstheresidualvertebratediversity
Ateachsite,duetothesupplyofequipment,wechosesevenfocalindividualsofFeijoa
basedonfruitpresenceand,asasecondaryfactor,thedistanceamongthemlargerthan150
m.Foreachfocalindividual,werecordedthefaunainthelowerstratum(~30cmfromthe
ground)usingacameratrap(Bushnell:TrophyCamHD,Model:119537c,BushnellOutdoor
ProductsCanada,Ontario,Canada),includingthreetemporalreplicasduring2015–2016
(autumninthebeginningof2015(TR1),middleofspringof2015(withoutfruits:TR2)and
autumninthebeginningof2016(TR3)).Forthefocalindividuals1,4and7ofeachsite,we
installedcameratrapsat(cid:21)1.7mhigh(upperstratum)andattachedfivefruitsoneachtree
withnails.Sinceistechnicallyimpossibleattachfruitinlocationsthattheywouldoccurnatu-
rally(e.g.,tipsofbranches),Feijoafruitswereattachedinatrunkcapableofreceivingthe
smallnails(12x12mm)andthatitwaspossibletoinstallthecameratrapimmediatelyahead
oftheseattachedfruits.Duetothenumberofavailablecameratraps,inTR2andTR3weonly
usedonecameratrapintheupperstratumthatwasinstalledonfocalindividualone.This
reductionincameratrapswithinupperstratumwaschosenbecauseaccordingtotheTR1the
mainfrugivoryactivitywasperformedonlowerstratum.Thus,wecankeeptheequalnumber
offocalindividual(seven)ineachtemporalreplica.
Weleftthecameratrapsactiveineachsiteforatleast30daysorfor60daysinsiteswhere
availablefruitsexceeded30days;inthesecases,after30daysweinspectedtheequipment.
Thus,atotalof40(or32)cameratrapswereused,programmedtorecordfootagefor45sec-
onds,withanintervalof45secondsbetweenrecordings,totaling4,470traps/day(Fig1).In
bothstrataandtemporalreplica,weanalyzedtheindependenceofinteractionsaccordingto
fruitsconsumed,withsequentialvideosofthesamespecies,whereconsumingthesamefruit
wasconsideredasingleinteractionrecord.Weestablishedthespectrumoffruitremovalby
thefollowingcriteria:(1)sinzoochory,thequantityofwholefruitstakenandtransportedaway
fromthelocation;and(2)endozoochory,fruitsconsumedlocally[47].Additionally,we
countedfruitremovalbysmallanimalsateachfocalindividualinTR1,using3-inchpipes
stucktotheground,whichcontained5Feijoafruits(prohibitingtheaccessofmediumtolarge
animals)(Fig1).
Resourceavailability,environmentalandspatialdata
Foreachtemporalreplicawithfruits(TR1andTR3),atthetimeofcameratrapinstallation
(t0),wecountedthenumberoffruitsavailableonthegroundbelowthecanopyofthefocal
individual.Weestimatedtheproductivityofeverytreebythenumberfruitsonthemain
branch(orentiretreewhenpossible)multipliedbythenumberofequal-sizedbranchesonthe
focalindividual(modifiedfromClarketal.2005)[54].Atintervalsof30days(t1)and60days
(t2),wereturnedtocounttheamountoffruitonthetreeandquantifiedfruitavailabilitydur-
ingcameratrapping.Int0,t1andt2,weweighedfivefruitsfromeachindividualwithaman-
ualprecisionbalance,andcalculatedthebiomassforeachtime.Furthermore,inTR1we:(1)
calculatedthefruitdecompositiontimeusing20fruitschosenrandomlyatasinglemoment,
leftunderconditionssimilartothesites;and(2)countedthenumberofseedsin15fruits.
Inthefirstyearofthestudy,werecordedthefocal-individualcanopyareaandthedistance
ofthefocalindividualtotheclosestFeijoaadult(withreproductivesignalsorcircumferenceat
breastheight(CBH)(cid:21)15cm)[55].Tocharacterizethesitehabitats,wemeasuredenviron-
mentalfeaturesusinganadaptedpointquadrant(S1Fig)method[56].Foreachfocalindivid-
ual,wemeasuredthecanopycoverpercentage(fromphotographstaken1.5mabovethe
ground,atfourpoints(N,S,EandW)fivemetersfromeachindividual),diameter,heightand
distancetothenearesttreeandshrub.Wealsoestimatedthepercentageofgroundcover(lit-
terfallandherbaceousgreencoverwithin1m2delimitedontheground),slope,orientation,
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Feijoadomesticationmaintainstheresidualvertebratediversity
intensityofuseoftheareabylivestock(ordinal:0(absence)to4(high))andactualhuman
presence(binary:0(low)and1(moderate)).
WealsonotedthepresenceofevidencesofmanagementinthefocalindividualsofFeijoa
(e.g.,tracesofpruning,treeandfruitsize,fruitvariety(e.g.,thinbark,moreappreciatedfor
localpeopleconsumes)andproximityofplaceswithpasthumanactivities),thatcanindicate
thecontinuityofdomesticationprocess[23,37,53](S1Fig).Wesupportedthisaforemen-
tionedinformationwithsemi-structuredquestionaries’appliedtolocalpeople[Bogonietal.
unpublisheddata].Thus,weobtainedaproportionofdomesticatedFeijoaswithinsitesbased
onqualitativedata.Forthis,weconsideredpresenceFeijoaswithmanagementevidence
(domesticatedFeijoas)andabsentforindividualsofFeijoa(“under-domesticated”Feijoas)
withinconspicuousdomesticationevidence,althoughitmaypresentatalowerlevel(e.g.,
molecular))[37,53].
Moreover,wedelimitedoneplotof1,600m2ineachsitetodeterminethedemographic
characteristics(accountofadults)ofFeijoawithinthesites(c).Wemeasuredlandscapechar-
acteristicsofthesitesandthedistancebetweenfocalindividualsandsitesthroughgeorefer-
enceddata.UsingGPS,satelliteimagesandQGissoftware[57],wemeasuredthelinear
distancefromthefocalindividualtotheclosestwatercourse,tothenearestopenareaandto
thenearestfragmentofnativeforest[58].Additionally,weobtainedthesize(asapolygon)of
theforestfragmentorlowland(i.e.,várzeaorflatareasofriverbanks,anenvironmentwhere
Feijoaoftenoccurs)basedoninsitupersonalobservationsandSantosetal.(2009)[23].
Dataanalysis
Weperformedaprincipalcomponentanalysis(PCA)ofcorrelationtoevaluatetheordination
samplingsitesacrossenvironmentalandlandscapeparameters,includingtheproportionof
managedFeijoatreeswithinsites[59–60].Descriptively,weexploredthespatialdistance,
demography,andfruitproductivityofFeijoaspersiteandtemporalreplicates(TR1andTR3),
usingcentraltendencyandvariationmeasures.Weanalyzedthestructureofthecommunities
usingdiversitydescriptors(i.e.,speciesrichnessandrarefactioncurveswithconfidenceinter-
valsof95%foreachreplica)[61–62].Foreachsite,weonlyusedindependentvideorecord-
ings,excludingrecordsofthesamespeciesatthesamefocalindividualfortimeintervals
shorterthan1hour[63],adjustedbysitesamplingeffort,andassumingspatialdependence
amongfocalindividualsformammalsandbirds.
Weanalyzedthetopologyofweightedtwo-modefrugivorynetworkspersiteforeachtem-
poralreplicateandperfocalindividual[64–65],inwhichasetofnodesrepresentingfrugivores
speciesisconnectedtoanothersetofnodesrepresentingsamplingsitesorfocalindividual
wheretheywererecordedconsumingFeijoafruits.Wecalculatedonequantitativemetric:
(a)modularity,andthreequalitative(binary)metrics:(b)averagedegree(c)connectanceand
(d)nestedness[66–67].Degreeisthenumberofinteractionseachnodehas.Modularity(M)
quantifiesthetendencyofthenodestoclusterintocohesivegroupsthataremoreconnected
amongthemselvesthanwiththerestofthenetwork[66].Connectanceistheproportionof
realizedlinks,thatistheratiobetweenthenumberofinteractionsobservedinrelationtothe
possibleinteractions[67].Nestedness(N)measuresthedegreebywhichthenestednetwork,
showingapossiblehierarchicalpattern[68].Incaseofnestedness,oneormoresitescanbea
subsetofothersiteswithlargestspeciesrichnessorlargestinteractionnumber.Formodular-
ity,weusedNewman’smetric[64]andcompareditsempiricalvaluewithabenchmark
distributionofmodularityvaluescalculatedtoanensembleof1000theoreticalmatricescre-
atedbyanullmodel,inwhichspeciesdegreerangesbetweenzeroandthemeanofthedegree
oftherealnetwork.Significance(p(cid:20)0.05)wasbasedontheratioatwhichlargerorequalto
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Feijoadomesticationmaintainstheresidualvertebratediversity
theobservedMvalueoccurredinthenullmodel[69].Fornestedness,weusedtheNODFmet-
ric[68].NODFrangesfromzero,whenthematrixisperfectlynon-nested,to100,whenthe
matrixisperfectlynested[70].WealsocomparedtheNODFvalueofempiricalnetworkwith
abenchmarkdistributiongeneratedby1000theoreticalmatricesgeneratedbyanullmodel
basedonaprobabilitymatrix(nullmodel2ofBascompteetal.2003)[69]andadoptingthe
sameaforementionedcriterionforMsignificance[69].Additionally,toshowresourcesharing
graphically,webuildthenetworkwiththedeconstructedinteractionspertemporalreplicain:
(1)dispersergroups(mammalsandbirds);(2)dispersalsyndromes(endozoochoryandsin-
zoochory);(3)verticalstrata(upperandlower);(4)time(t0tot1andt1tot2);and(5)circa-
diancondition(dayandnight).
Weperformedavariationpartitioninganalysistoassesstheenvironmental(includingFei-
joadomesticationevidence),spatialdistanceandproductivityvariationeffectsoninteractions
[59–60]atthefocalindividualscale,consideringthetwogroups(nativemammalsandbirds)
separated.However,apriori,weconductedaprincipalcomponentanalysisofneighboring
arrays(PCNM)todeterminesignificantspatialcomponentsobtainedbythearrayofdistance
betweenfocalindividuals.ThePCNMsrepresentthespatialrelationshipbetweensampling
sitesandcanbeusedaspredictorsofvariation.OnlypositivePCNMswereselectedaccording
tospatialautocorrelationobtainedbyMoran’sindex[59–60].
Topartitionthevariation,weusedtheforwardselectionmethod(toreducethelikelihood
ofatypeIerror)[71]toselectasubsetofsignificantpredictorvariablesbasedonthenon-mul-
ticollineardata(testedaprioriviathevarianceinflationfactors)[72].Variationpartitioning
performsRDAsforallpredictors,andindividuallyforeachsetofpredictors,removingeffects
ofotherpredictors(e.g.,RDAfortheenvironmentremoveseffectsofspatialdistance).The
proportionsexplainedbypredictorswererepresentedbyEzekiel-adjustedR2[73].Forthevar-
iationpartitioning,wecorrectedtheasymmetryintheinteractionnumberusingHellinger
transformation.Theasymmetryoftheenvironmentandlandscapefeatures(numericalmagni-
tudes)wastransformedbystandardization,andtheresourceavailability(totalbiomass)was
logarithmized[60].Webasedthesignificanceofvariationpartitioningtests(p(cid:20)0.05)on999
permutations.Forotheranalyses,usedtheoriginal,untransformeddatasets.Weperformedall
analysesinR[74]withthesna[75],bipartite[76],vegan[77]andPackfor[78]packages.
Results
Environment,spatialdistancesanddemographicfeatures
Environmentandlandscapefeatures,analyzedviaPCA,explained85.4%oftotaldatavariation
amongsites,with52.7%oftheexplanationrelatedtoaxisone(linkedmainlytoslopeandlow-
land/fragmentsize)and32.7%ofexplanationrelatedtoaxistwo(linkedtotreeheightanddis-
tancetonearestfragment).Thesitesaredistinctinthefollowingaspects:S1isthefurthest
fromawatercourse(340m);S2hashigheradultdensity(eachoneby5.5mapart);S3,besides
theintensepresenceofcattle,ischaracterizedbythegreaterarea(697ha)of“várzea”;andS4
isthefurthestfromanopenarea(105m)(S2Fig).Althoughnotthemainfactorintheordina-
tionanalysis,atdifferentintensitiesorreplications,therewasarealorvirtualpresenceofcattle
inallsites.Theaveragedistancebetweensitesis23.7km(±11.3;1.6to34.3km).Thedistance
amongfocalindividualsis261.5m(±182.4;11.3to496.5m)inS1,446.7m(±320.9;11.2to
1000m)inS2,346.4m(±246.7;7.7to716m)inS3,and584.9m(±356.4;88to1167m)inS4.
Consideringallsites,andbasedonthedistanceamongFeijoatreesanddemographicplots,
thereisanaverageof48.8(±39.8)Feijoaadultsperhectare.TheproportionofFeijoatrees
(focalindividuals)withclearevidenceofpastmanagement(i.e.domestication)was85.7%(6
in7)inS1,57%(4in7)inS2andS4and0%inS3(Table1).
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Feijoadomesticationmaintainstheresidualvertebratediversity
Table1. Density,domesticationevidence,andproductivityofAccasellowianaatfoursitesandtwotemporalreplicaswithfruitsinsubtropicalAtlanticForesthigh-
lands,Brazil. S1andS2:SãoJoaquimNationalPark;S3:surroundingofRPPNGrandeFlorestadasArauca´rias;andS4:RPPNLeãodaMontanha;A:adults.
Replica Density Domesticationevidence Fruits Biomass
Spatial Temporal Ind/ha(A) Nin7focalindividuals(%) Ntotal/Site(±SD) Ntotal/ha(±SD) Average(g/fruit(±SD)) Kg/Site Kg/ha
S1 TR1 - 2,661 14,255.3 46.2(16.5) 123.7 662.7
TR3 - 924 4,950 24.2(12.1) 22.4 120.0
Mean 37.5 6/7(85.7%) 1,792.5(1,228.2) 9,602.7(6,580) 35.2(15.6) 73.1(71.3) 391.4(383)
S2 TR1 - 844 1,700.1 30.6(7.9) 25.8 52.0
TR3 - 72 145.1 27.4(15.1) 1.9 3.8
Mean 14.1 4/7(57%) 458(545.9) 922.6(1,100) 29.0(2.3) 13.9(16.9) 27.9(34)
S3 TR1 - 313 4,753.2 28.1(14.4) 8.8 133.6
TR3 - 96 1,457.8 12.8(6.2) 1.2 18.2
Mean 106.3 0/7(0%) 204.5(153.4) 3,105.5(2,330) 20.5(10.8) 5.0(5.4) 75.9(82)
S4 TR1 - 696 3728.6 39.8(15.8) 34.8 186.4
TR3 - 369 1976.8 27.2(11.9) 10.0 53.6
Mean 37.5 4/7(57%) 532.5(231.2) 2,852.7(1,239) 33.5(9.0) 22.4(17.5) 120.0(94)
Average 48.8(39.8) 50(36) 746.9(838.1) 4,120.9(3,782.4) 29.6(10.0) 28.6(40.2) 153.8(162.8)
https://doi.org/10.1371/journal.pone.0195199.t001
Productivityandinteractions
Spatially,theproductivityamongsitesvariedfromdozenstomorethan2,500fruits(average
746.9;SD±838.1;totaling5,975fruits),andthebiomasswasalsohighlyvariable(3.03±5.98kg
perindividual;28.6±40.2persite)(S3Fig).Thesevalues,extrapolatedforthedensityofadults
perhectare,maintainedhighspatialvariation(4,120.9±3782.4fruits/ha-1and153.8±162.8kg/
ha-1)withmajorproductivityinS1andS4.Temporally,wealsofoundhighvariationinthe
numberoffruitsandbiomass,witha67.6%decreaseinfruitavailabilitybetweenTR3with
TR1(Table1).Thefruitsrottedinnine(±2.4)daysandtheaveragenumberofseedsperfruit
was61.9(±36.4).
Cameratrapsrecordedatotalof1,948videos(1,461minutes),including470independent
interactionsand1,141independentrecordsaccordingtobothourcriteria,with37nativespe-
ciesrecordedwhenconsideringCricetidaeasauniquespecies(S2Table).Rarefactioncurves
consideringallthenativespeciesrecorded(independentlyofinteractionwithFeijoa)showed
therewasasignificanttemporaldifferenceinspeciesrichness,i.e.,betweenpresence(TR1and
TR3)andabsence(TR2)oftheresourcewhencomparingaminimumofindependentrecords
(S1:72;disregardingS3duelowrichness).However,amongsites,therewasnosignificantdif-
ferenceinrichness,withconfidenceintervalsoverlapping,exceptforS3(Fig2).Thispattern
wasmaintainedwhenthetemporalreplicaswereseparate(Fig2;S4Fig).
Duringthetwoyearsofsampling,20species(includingcattleandCricetidae:S5FigandS1
MovieFile)interactedwithFeijoa,withanaveragesitesdegreeof14.41(±10.1),aFeijoafruit
removalof9.6%representing572fruitsremovedandmorethan35,400seeds.Amongsites,
whenbothtemporalreplicaswerecombinedtheremovalproportionwere3.35%forS1,
27.84%forS2,13.70%forS3and12.77%forS4.InTR1,theaverageremovalwas14.39%
(3.2%to28.1%amongsites,withthesamepatternasthetotalaverage)madeby19species:
2.83%by10nativemammals(includingCricetidae),7.28%byeightnativebirds,and4.29%by
cattle.InTR3,theaverageremovalwas13.41%(3.57to25.0%amongsites)madeby13species:
7.80%byeightnativemammals,2.75%byfournativebirdsand2.86%bycattle(Fig3).
Amongnativemammals,Cricetidae(speciesdegreeof6.09),Eirabarbara(1.91),Cerdocyon
thous(1.88),Nasuanasua(1.66)andDidelphisaurita(1.05)arethemainspeciesthatremove
fruits.Aramidessaracura(22.76),Penelopeobscura(2.05),Pyrrhurafrontalis(1.50),Turdus
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Feijoadomesticationmaintainstheresidualvertebratediversity
Fig2. (A)Rarefactioncurve(withaconfidenceintervalof95%ingray)forallindependentrecords(consideringtwo
replicaswithfruitandonewithoutfruits)ofmammalandbirdspecies(exceptexotic)duringevaluationoffruit
removalfromAccasellowianainfoursitesinsubtropicalAtlanticForesthighlands,Brazil;(B)Rarefactionbyspatial
andtemporalreplicasforallindependentrecordsofmammalsandbirdsspecies(exceptexoticspecies)during
evaluationoffruitremovalfromAccasellowianainfoursitesinsubtropicalAtlanticForesthighlands,Brazil.
Independentrecordswereadjustedbysamplingeffort(camera-trap/day/replica).S1andS2:SãoJoaquimNational
Park;S3:surroundingofRPPNGrandeFlorestadasArauca´rias;andS4:RPPNLeãodaMontanha.
https://doi.org/10.1371/journal.pone.0195199.g002
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