Collaborative management as a way to enhance Araucaria Forest resilience

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SupportedbyBotic´arioGroupFoundationforNatureProtection

www.perspectecolconserv.com

Essays

and

Perspectives

Collaborative

management

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enhance

Araucaria

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resilience

Mario

M. Tagliari

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_Carolina

_Levis

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_Bernardo

_M.

_Flores

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_Graziela

_D.

_Blanco

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_Carolina

_T.

_Freitas

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Juliano

A. Bogoni

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_Ghislain

_Vieilledent

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_Nivaldo

_Peroni

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a_Programa_de_{Pós-graduac¸}_ão_em_Ecologia,_Departamento_de_Zoologia_e_Ecologia,_Universidade_Federal_de_Santa_Catarina,_{Florianópolis,}_Brazil

b_CIRAD,_UMR_AMAP,_AMAP,_Univ_Montpellier,_CIRAD,_CNRS,_INRAE,_IRD,_F-34398_Montpellier,_France

c_Divisão_de_{Sensoriamento}_Remoto,_Coordenac¸_ão_de_Observac¸_ão_da_Terra,_Instituto_Nacional_de_Pesquisas_Espaciais,_São_José_dos_Campos,_SP,_Brazil

d_School_of_{Environmental}_Sciences,_University_of_East_Anglia,_Norwich_NR4_7TJ,_UK

e_Universidade_de_São_Paulo,_Escola_Superior_de_Agricultura_“Luiz_de_Queiroz”,_Laboratório_de_Ecologia,_Manejo_e_Conservac¸_ão_de_Fauna_Silvestre_(LEMaC),_Piracicaba,_São_Paulo,_Brazil

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•Top-down restrictive measures are thebasisofAraucariaForestSystem conservation

•Bottom-up collaborative manage-ment could favor keystone plant Araucariaangustifolia

•Top-downmodelhadnegative feed-backthatdampensthesystem limit-ingitsresilience

•Bottom-upmodelhadpositive feed-backexpandingthesystemand its generalresilience

•Collaborative management could maintain the Araucaria Forests Systeminthelongterm

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Articlehistory: Received7September2020 Accepted1March2021 Availableonlinexxx Keywords:

AraucariaForestSystem

Culturalkeystonespecies

EcologicalKeystoneSpecies

Ethnoecology

MixedOmbrophilousForest

Participatoryconservation

Resilience-thinking.

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Peopleandnatureinteractsincemillenniainforestsworldwide,butcurrentmanagementstrategies addressingtheseecosystemsoftenexcludelocalpeoplefromthedecision-makingprocess.Thistop-down approachisthecornerstoneofconservationinitiatives,particularlyinhighlythreatenedandfragmented forestedecosystems.Incontrast,collaborativemanagementinvolvingtheparticipationoflocal com-munitieshasincreasinglycontributedtoconservationeffortsglobally.Hereweaskhowcollaborative managementwouldcontributetotheconservationofathreatened,culturallyimportant,andkeystone treespecies.WeaddressthisquestionintheAraucariaForestSystem1_(AFS)_in_southern_Brazil,_where_the mainconservationstrategyhasbeentop-downbasedonrestrictiveuse.Throughouttheentire distribu-tionofAFS,weinterviewed97smallholdersabouthowtheyuseandmanageAraucariaangustifoliatrees (araucaria).WeintegratedtheirTraditionalEcologicalKnowledge2_(TEK)_with_a_literature_review_about theconservationstatusofAraucariaForeststoanalyzepotentialoutcomesoftwoalternativeconservation models:top-downwithrestrictiveuse,andbottom-upwithcollaborativemanagement.Weidentiﬁed thefeedbackmechanismsineachmodel,andhowtheydampenorself-reinforcedcriticalprocessesfor AFSresilience.Ourmodelsshowedthatatop-downstrategymaintainsforestcoverresilienttoillegal loggingbutatthecostoflosingTEK(underminingsocio-ecologicalresilience)andforestresilienceto

∗ Correspondingauthor.

E-mailaddress:[email protected](M.M.Tagliari).

1_Araucaria_Forest_System_–_AFS

2_Traditional_Ecological_Knowledge_–_TEK

https://doi.org/10.1016/j.pecon.2021.03.002

creativecommons.org/licenses/by-nc-nd/4.0/).

Pleasecitethisarticleas:M.M.Tagliari,C.Levis,B.M.Floresetal.CollaborativemanagementasawaytoenhanceAraucariaForest resilience,PerspectivesinEcologyandConservation,https://doi.org/10.1016/j.pecon.2021.03.002

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otherexternaldisturbances,suchasclimatechange.Alternatively,abottom-upapproachbasedon suc-cessfulcollaborativemanagementschemesmayincreasethegeneralresilienceofAFS,whilepreserving TEK,thuscontributingtomaintainingtheentiresocial-ecologicalsystem.Ourﬁndingsindicatehowit isparamounttomaintainTEKtoconserveAFSinthelongtermthroughcollaborativemanagement.By includinglocalactorsinthegovernanceofAFS,itsresilienceisreinforced,promotingforestexpansion, maintenanceofTEK,andparticipatoryconservation.

INTRODUCTION

In the human-in-nature perspective, Social-Ecological Sys-tems(hereafterSES)aretheintegrationofhumansocietieswith ecosystemspromotingreciprocalfeedbacks,interdependence,and resilience(Folkeetal.,2010).TheresilienceofSESdependsontheir abilitytoadaptandremainwithinastabilitydomaininthefaceof disturbancesandexternalstressors,i.e.itdoesnotmovebeyond thresholdstoanalternativestateofequilibrium.Theadaptability ofSESenhancesitsresiliencebecauseitallowsthesystemtoadjust itselfinthefaceofadversities(Berkesetal.,2000).Forests world-wideareperfectexamplesofSESgiventhelong-terminteraction betweenforests,plants,andpeoples.Inthelargestconservedblock oftropicalforestintheworld–theAmazonforest,forinstance, multiplehumanmanagementpracticesovermillenniaincreased edibleplantdiversityandabundancewithinforestpatches, partic-ularlyneartoarchaeologicalsites,contributingtoenhancingfood securityandproduction(Levisetal.,2018).

One of themost emblematicSES of thesubtropical Atlantic ForestistheAraucariaForestSystem(hereafterAFS),alsoknown asAraucariaMixedForest(Fig.1).First,becauseofitsdominant species,thecandelabra-aspecttreeAraucariaangustifolia(Bertol.) Kuntze, popularly known as araucaria, has a keystone role in ecosystemfunctioning,especiallyduetoitsnut-likeseed,known as‘pinhão’,whichstructurestheassociatevertebrateassemblage spatio-temporally(Bogonietal.,2020;Oliveira-Filhoetal.,2015).

Fig.1.SchemeoftheAraucariaForestSystem(adaptedfromBogonietal.,2020).1.

TheAraucariaecologicalsystem.Thearaucaria(candelabratree)andthetypical

ecologicalsystemunderitscanopy,suchasOcoteasp.–“Canela”;Ilexparaguariensis

–“erva-mate”;Dicksoniasellowiana–“xaxim”;andAccasellowiana–

“goiabeira-serrana”;andrepresentativefauna,suchastheMazamagouazoubira –“veado

campeiro”;Pumaconcolor–“cougar”;Dasyproctaazarae–“cutia”;andCyanocorax

caeruleus–“azureJaybird”.2.TheAraucariasocio-ecologicalsystem.We

repre-sentedthecurrentscenarioofaraucariaremnants,especiallyinsouthernBrazil,

wherelocalgroups(smallholders;indigenouspeoples)continuetomanagethe

systemsincepre-Columbiantimes.

Second,becauseofitsancientconnectionwithIndigenouspeoples andlocalcommunities(IPLCs;Reisetal.,2014;Robinson etal., 2018). The araucaria wasand still is widelyused by local and indigenousgroupsdue totheconsumption ofpinhão(Robinson etal.,2018),withhighcaloriccontentthathelpscopingwiththe winterseasons(MelloandPeroni,2015).Araucariaseedsarepart ofintensetraditionaluse,management,andcommerceby small-holdersas wellas pinhão extractorsacrossdifferent regions of Southernand SoutheasternBrazil(Adanetal.,2016; Melloand Peroni,2015;Reisetal.,2014;Quinteiroetal.,2019;Tagliariand Peroni,2018;Zechinietal.,2018).Thecomprehensionthat cer-tainspeciesarecrucialtomaintainingdifferentcultures,suchas smallholdersorindigenousgroups,wasthebasistocreatetheterm “CulturalKeystoneSpecies”(GaribaldiandTurner,2004).Herewe useasimilarterm“culturallyimportantspecies”,followingFreitas etal.(2020),whichconsidersthespeciesoverridingroleinpeople’s culture,althoughnotnecessarilyindispensableforthesurvivalof a speciﬁcculture. However,if a culturally important species is extinctlocallyorhassufferedapopulationdecline,itwillstrictly inﬂuencelocalpeoples’subsistenceandspirituality(Freitasetal., 2020),aswellasthetransmissionofTraditionalEcological Knowl-edge(Berkes,2009).Yet,giventheintensecommercialexploitation ofA.angustifoliaduringthe20th _century_due_to_its_high-quality

wood(WendlingandZanette,2017),thespeciesiscurrently classi-ﬁedas“CriticallyEndangered”accordingtotheInternationalUnion forConservationofNature(IUCN,Thomas,2013).Sincethen,the Brazilian legislation forbids anyforms of araucaria logging and stimulatesthecreationandmaintenanceoftop-downprotective strategies.Asaresult,StrictlyProtectedareasarethecornerstoneof conservationstrategiesrelatedtoAraucariaForestSystems,which oftenexcludelocalandindigenouspeoplesfromparticipatingin biodiversityconservation(Zechinietal.,2018).

ProtectedAreas(PA)arewell-known refugesforbiodiversity andecosystems,particularlyintheAtlanticForest,wheremostof thesystempersistsinfragmentssurroundedbydenselyinhabited urbanandruralareas(ScaranoandCeotto,2015;Pachecoetal., 2018;Metzgeretal.,2019).AlthoughProtectedAreasencompass only4%to6%ofthecurrentAraucariaForestextent(Castroetal., 2019;Ribeiroetal.,2009), studiesevaluatingtheireffectiveness foraraucariaconservation(Castroetal.,2019)didnottakeinto accountanothermajorcategory:LegalReserves– aspecial pri-vatePA.ThesecompulsoryprivatePAshostalmostone-thirdofall remainingnativevegetationintheAtlanticForest(Metzgeretal., 2019).MostofthenativeAraucariaForestfragmentsoccurwithin smallfarms(BittencourtandSebbenn,2009).Consequently,itis undeniablethatlocalsmallholdersalsocontributetopreserving, willinglyorunwillingly,theAraucariaForests.However,previous ethnoecologicalsurveyshavesuggestedthattop-downstrategies (i.e.maintenance andcreationofStrictlyPublicProtectedAreas andPrivateProtectedAreas)maynegativelyimpactthe interac-tionsbetweensmallholdersandaraucariatrees(Adanetal.,2016;

TagliariandPeroni,2018).Forinstance,becauseremoving arau-cariatreesisillegal,somelandownersdonotdependonaraucaria’s resources,andthusarepronetoactivelypreventaraucaria’s nat-uralregenerationbyremovingitsseedlingsfromtheirproperties beforetheyreachmaturity(Adanetal.,2016;MelloandPeroni, 2015;Quinteiroetal.,2019;TagliariandPeroni,2018).Inthiscase,

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livestockfarming(e.g.cattle),pastureorcropproductionfor sub-sistence,suchascornormanioc,usuallycompetewitharaucaria’s naturalregeneration,creatingahuman-plantbarrier(Adanetal., 2016;TagliariandPeroni,2018),wheresomelandownersstatethat theylosetherightstousetheirlandsbecauseofprotectedspecies (Quinteiroetal.,2019).

The araucaria case is therefore a conservation dilemma: people and natural resources interact since millennia, but cur-rent management strategies often exclude local people from thedecision-making process.Top-down strategiespreventlocal engagement in AraucariaForest conservation. Furthermore,the contributionoftop-downconservationstrategiestothelong-term conservationofnature,individuallyorglobally,stilllacks effective-ness(RodriguesandCazalis,2020),especiallyregardingpotential limitations totheprotectedareaperse,suchassocio-ecological resilienceorclimatechangeimpacts(Ferroetal.,2014).In con-trast,bottom-upstrategies,developedtogetherwithlocalhuman groupsthroughsharingdecisionsbetweengovernments, institu-tionsandlocalresourceusersaremorelikelytoproducebeneﬁts forthesocial-ecologicalsystemasawhole,besidesstrengthening ecosystemresilience(Folkeetal.,2010;Bennettetal.,2016).

From the human-inﬂuenced expansion of Araucaria Forests during the past two millennia (Robinson et al., 2018) to the currenthighlyproductivesystems–suchasthe“faxinais”– under-neatharaucariacanopies,combinedwithIlexparaguariensis,locally knownas“yerba-mate”,atraditionaltea-likebeverage(Reisetal., 2018),humansarepartoftheAraucariaForestSystem(Reisetal., 2014).Themaintenanceoftraditionalpracticesconstitutesa gen-erational body of knowledge, beliefs, and practices, known as TraditionalEcologicalKnowledge(TEK;sensuBerkes,2009),which is fundamental for the persistence of social-ecological systems (Folkeetal.,2005).Inpractice,localsocietiesthatmanage ecosys-temsbasedonTEKcontributetomaintainingculturallyimportant species aswell ashuman cultures resilient by a positive feed-backmechanism(Cámara-Leretetal.,2019),andbydoingso,this processalsomaintainstheecosystemresilient,particularlyif man-agementaddressesakeystonespeciessuchasaraucaria(Bogoni etal.,2020).Consequently,acrucialsteptomaintainingthe Arau-cariaForestSystemresilientisbymanagingthefeedbackswithin itssystem(Biggsetal.,2012;Musavengane,2019;andseeFig.1

comparingtheAraucariaecologicalandsocio-ecologicalsystem). Feedbacksareinteractionsinwhichtheresultingeffecteither reinforces (positive) or dampens (negative) change (DeAngelis etal.,1986),influencingecosystemdynamics.Forinstance,when treesestablishinafire-pronesavannalandscape,theyreducefire spread, favoring forest expansion(vanNes et al. 2018). Partic-ularly, thepositive feedbacks,which self-reinforcechanges, are capable of triggeringcascadingeffects that push entire ecosys-temstoalternativestates(Estesetal.,2011;Schefferetal.,2001). Feedbacksdepicttheecologicalprocessesthatpromoteordegrade ecosystemresilienceandfunctioning;andhencearethekey mech-anismstobeincorporatedinecosystemmanagement(Briskeetal., 2006).Bothpositiveandnegativefeedbacksplaymajorrolesinthe self-organizationofsocial-ecologicalsystems.Therefore,to man-ageresilienceit isnecessarytounderstandthemostimportant feedbacksinthesystem,especiallyinvulnerableandthreatened ecosystems,suchasAraucariaForests(Briskeetal.,2006)where localpeopleswithdeepecologicalknowledgearelikelytobe crit-icalpartners.

Collaborativemanagement(co-management)impliesa partic-ipatory decision-making process in which the management of a natural resource is shared between users and other actors, suchasnational,andsubnationalgovernments,Non-Governmental Organizations (NGOs), and/or local cooperatives (Berkes and Davidson-Hunt, 2006). Garibaldi and Turner (2004) argue that if local peopleidentifythemselves witha certainspecies, they

willhavea strongdesiretopreserveorrestoreit. Preservinga culturallyimportant species, therefore,may guarantee the par-ticipationof differentactors in species’ conservationprograms, andconsequentlybeneﬁtboth thespecies,localpeople,andits surroundingecosystem (Cristancho and Vining, 2004;Garibaldi andTurner,2004;Nobleetal.,2016).Althoughstudiesaddressing co-managementschemesofculturallyimportantspeciesremain scarce in the literature due to the lack of ecological, social, andeconomicquantitativedata,thisbottom-upapproachseems promising to effectively engage local people into conservation actions(Freitasetal.,2020).Furthermore,co-managementmaybe partofresilience-thinkingbecauseitincorporatessomeofitsmain principles,accordingtoStockholmResilienceCentre(Stockholm ResilienceCentre,2013),suchasthemanagementoffeedbacksand theparticipationoflocalsinthegovernanceofthesocial-ecological system.

Applyingresilience-thinkingtolocalorregionalconservation issuesisstillagreatchallengebecausedecision-makersare usu-allyattached to traditional conservation strategies. In thecase ofAraucariaForestSystems,wherethemainconservation strat-egyisfocusedonatop-downconservationmodelwithrestrictive use,uncertaintiesstillexistwhetheracollaborativemanagement scheme could contribute to improving conservation outcomes. Herewe addressthis dilemmaina broadscalestudy toobtain detailedinformationonthestateoftheAraucariaForestSystem andunderstandhowbothtop-downandbottom-upconservation strategiesmayaffecttheresilienceofthissystem,includingits cul-turalandecologicaldimensions.First,basedonacomprehensive literaturereview,weanalyzefeedbacksandtheresulting dynam-icsoftwoalternativeconservationmodels:(1)top-downunder restrictiveuseand(2)bottom-upwithco-managementschemes. Second,based onevidence from97 semi-structured interviews withsmallholdersacrosstheAraucariaForest, weexploredthe risksandbeneﬁtsofimplementingbothmodels.Bypresentingthe keyinteractionsandfeedbacksthatcouldstrengthenlocal engage-mentforaraucariaconservation,weexpecttoprovidea critical perspectiveformanagingandenhancingAraucariaForestSystem resilience.

METHODS

Studyarea

ThestudywasconductedinsouthernBrazil,acrosstheentire extentoftheAraucariaForestecoregion(Fig.2)andcoveringfour environments:Alluvial-onoldterracesassociatedwiththeriver system;Sub-montane-constitutingdisjunctionsataltitudesbelow 400m;Montane-locatedapproximatelybetween400and1000 mof altitude; and High Montane - comprising altitudes above 1000m(IBGE,2012).Thehighlandclimate,wheretheescarpment rises ∼1000m fromtheAtlantic Forest coastalplain,is humid mesothermic;temperature range between15-20◦C;and mean annualrainfallof 1500-2000mm (Robinson etal.,2018).Atits northeasternlimit,theecoregionexperiencesa tropicalclimate, andpersistsonlyatspeciﬁccoldtemperaturesspotsathigher alti-tudes,suchasMantiqueirahills,attheHighRioPretoMicrobasin (Castroetal.,2019;Quinteiroetal.,2019).

Araucariapoliciesandlegislation

Severalcategoriesof protectedareas exist inBrazil: Conser-vationUnits,whicharedividedintoStrictlyProtectedAreasand SustainableUseAreas,andaremanagedbyfederal,state,or munici-paladministration,orthroughpartnershipswiththeprivatesector (DeMouraetal.,2009);PermanentPreservationAreasandLegal

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Fig.2. (a)TheAtlanticForest(darkgray)withtheAraucariaForestecoregion(green)showingthethreeBrazilianstateswhichmainlyencompasstheecoregion:Paraná

(PR),SantaCatarina(SC),andRioGrandedoSul(RS);(b)TheAraucariaForestaltitudemapandthedistributionofConservationUnits:Strictly(yellow)andSustainableUse

ProtectedAreas(green);blackdotsrepresenttheoccurrenceof97ethnoecologicalinterviewsinthisstudy.WehighlightthatthreeinterviewsoccurredatSãoPaulostate

(beyondtheAraucariaForestecoregion)atCunhamunicipality.

Reserves(privateprotectedareaswithinprivateproperties);and IndigenousLands(Pachecoetal.,2018).AccordingtotheBrazilian NationalSystemofConservationUnits(BRASIL,2000),the Sustain-ableUsecategoryisdividedintosevensub-categories,ofwhich two couldbespeciallytargetedtoTEKholdersintheAraucaria Forest System: Sustainable Development Reserves and Extrac-tiveReserves.Bothtypesofprotectedareasaimtosafeguardthe livelihoodsandculturesoftraditionalsocialgroups,aswellasto conservenatureanditsbiodiversity(DeMouraetal.,2009).Also, ExtractiveReservesrequiresomelevelofcommunityorganization andcooperation.

However,only10.6%oftheAtlanticForest(thusincludingthe AFS)isencompassedbyConservationUnits,mostlyofSustainable Use(75%).Furthermore,fromthe75%ofSustainableUse Conser-vationUnitscreatedwithintheAtlanticForest,only0.45%and0.62 %areclassiﬁedasSustainableDevelopmentReservesand Extrac-tiveReserves,respectively(Pachecoetal.,2018).Asaresult,few protectedareasintheAFSrecognizetheimportanceoftraditional peoples.Also,SustainableUseConservationUnitsaremanagedby thestategovernments,contrarytoStrictlyProtectedAreas– man-agedbyFederalgovernment–;andIndigenousLands,whichcover only0.72%oftheAFSarea(Pachecoetal.,2018),areadministered bytheFederalIndianAgency–FUNAI.Finally,almostone-thirdof AtlanticForest’sremainingnativevegetationoccurswithinLegal ReservesandPermanentPreservationAreas,inprivateproperties (Metzgeretal.,2019).Consequently,mostofthenativeAraucaria Forestoccurswithinsmallfarms(BittencourtandSebbenn,2009) anditisinspectedbymunicipal,state,andfederalagencies.Farmers whouseandmanagearaucaria’sresourcesareusuallylow-income smallholderswhodonotreceiveanyﬁnancialreturnfor conserv-ingforestedareas(OrellanaandVanclay,2018).Thelackofpolitical incentivesforAraucariaForest’sactivemanagementhasledto ille-galland-usepracticeswithinLegalReserves(OrellanaandVanclay, 2018).

TheBrazilianlegislationprohibitsanytypeofmanagementof araucaria timber(Lei daMata Atlântica or Atlantic Forest Law n◦11.428/2006;CONAMAResolutionn◦278/2001).However,the ParanáStaterecentlyapprovedanewLawn◦20.223/2020(Paraná OfﬁcialDiary,2020),whichregulatestheplantingandexploitation ofAraucariaangustifolia,aimingtostimulatetimbermanagement programs.Thisnewlawdeﬁnesandauthorizestimberexploitation inprivatepropertiesbeyondrestrictedareas(e.g.LegalReserves)

andareaswhereillegaldeforestationpreviouslyoccurredwithin theAtlanticForest.Yet,bypromotingonlytimberexploitation,a newmarketiscreatedforaraucaria,possiblystimulatinglocal pop-ulationsunderTEKsystemstoabandontheirancientpractices.This alternativeeconomicactivitybeneﬁtslandownersbutmay under-minetheresilienceofthesocial-ecologicalsysteminthelong-term. Wehighlightthatlegislationshouldalsopromote,inthissense,the maintenanceofAraucariaForeststands(“FlorestaemPé”)beyond LegalReservesaspotentialareas forco-managementinitiatives viaPaymentforEnvironmentalServices(Tagliarietal.,2019). Sus-tainablepinhãoproductionandAraucariaForestreforestationare someoftheexistingprojectsunderthepossibilitiesofPaymentfor EnvironmentalServices(seeTagliarietal.,2019).

TheTraditionalEcologicalKnowledgeholdersinthecontextofthe study

Within the AFS different actors use, manage, and explore araucariaresources as opposingtoother social groups who do notusethem.DespitehumanmanagementsincePre-Columbian times,whereethnicgroupscultivatedpinhãoforsubsistenceand religiousness(Reisetal.,2014),duringthe20th_century,_a

combi-nationofagricultureexpansion,urbanization,andloggingchanged abruptlytheAFS(Rezendeetal.,2018;Ribeiroetal.,2009). Log-gingwasespeciallyrelevanttodecimate97%ofaraucariaremnant populationssincethebeginningofthe20th_century₍_Enright_and Hill,1995).Thisexploratoryscenarioculminatedinseveral restric-tivemeasures,suchasloggingprohibition,toprotectthe‘Critically Endangered’speciesfortheIUCNRedList(Thomasetal.,2013).

InAFS,manysocialgroupsuseandmanagearaucariaresources, butother social groupsdo not useormanage them. Thelatter reliesmainlyonlivestock, agriculture,and farmingsystems for commerce and subsistence, while smallholders who use Arau-cariaForestSystems dependeconomicallyonpinhãoextraction andotherassociatedcrops(e.g.,tobaccoandyerba-mate)fortheir livelihoods(Adanetal.,2016;Quinteiroetal.,2019;Tagliariand Peroni,2018).Thisinteractionbetweentraditionalsmallholders andAFSusuallysurpassesmorethanonegeneration,becausethey werebornandraisedinthesamefamily’sproperties(Adanetal., 2016),wheretheymightlearntheprocessesofcommunity orga-nizationandcooperation(Reisetal.,2018).Wethusdeﬁnedthe speciﬁcgroupof smallholdersand pinhãoextractorsdistributed

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acrossSouthernandSoutheasternBrazilasTraditionalEcological Knowledgeholdersinthecontextofthestudy.Thisattribute indi-catesknowledge,use,anddependencyonaraucariamanagement. Weproceededwiththeapplicationofthesemi-structured ques-tionnairewithTEKholders.Potentialparticipantswereindicated byinformalconversations withsmallholdersandpinhão extrac-torsineachmunicipalityandwithenvironmentalspecialists(such asmunicipalitiesorStateenvironmentsbureaus,professors,and universities).Weappliedthesnowballtechnique(Bernard,2006) to followthe semi-structuredinterviews, where participantsat theendoftheinterviewrecommendedpeopledirectlyinvolved inaraucariamanagement.Werecognizethatindigenouspeoples, such as Southern-Jê and Guarani, have shaped remnant forest composition in SouthernBrazil(Cruz etal.,2020), and arealso importantTEKholders.However,duetoethicalaspectsandlegal authorizationwedidnotincludeindigenouspeoplesinourstudy. Datacollectionfromethnoecologicalinterviewsandtheliterature

Weconductedtwostrategiesfordatacollectionfromthestudy area:fieldworkandacomprehensiveliteraturereview.To quan-titatively assess the aspects of araucaria co-management with local smallholders and araucaria nut-like seeds extractors, we first identified key-regionsinSouthern and SoutheasternBrazil where pinhão use, commerce, and management are commonly described (e.g.regionalpinhãoparties,suchas“FestadoPinhão” at Lages and Cunha municipalities; informal pinhão commerce along estate highways; andpublishedliterature). We thus con-ducted97semi-structuredinterviewswithkey-informantsinfour Brazilian States:Paraná,SantaCatarina,Rio GrandedoSul,and São Paulo (surroundings of Mantiqueira hills at Cunha munic-ipality), covering 14 municipalities between March 2018 and January2019(Fig.2).Priortotheapplicationofthequestionnaire totheparticipants,weobtainedinterviewees’consentfollowing the codeof ethics ofthe InternationalSociety of Ethnobiology. Our study was approved by the ethics committee of the Fed-eralUniversityofSantaCatarina(CAEE:86394518.0.0000.0121). Thesemi-structuredinterviewprotocoladdressedthreemain top-ics:(i)historicalmanagementandsocioeconomicfactors;(ii)the araucariaecologyandethnoecologyaspects;(iii)interviewees’ per-spectivesaboutclimatechangethreatsforaraucaria(seeTable1

andTableS1).Toassessthelocalknowledgeandstate-of-the-artof araucariaco-managementforthisstudy,weselectedspeciﬁc open-endedquestionsthroughthequestionnairesuchas(i)“Whatisthe importanceofpinhãotoyourproperty?”;(ii)“Whatarethecauses behindtheexpansion/retractioninaraucaria’spopulation?”;(iii) “How muchpinhão (kg)hasbeengatheredinyour propertyon average?”; (iv)“How many ethnovarieties ofaraucaria canyou identifyinthelandscape?”;(v)Whatarethedifferencesinsize, color, taste,ripeningperiod oftheethnovarieties? (vi)“Doyou practiceanymanagementduringpinhãogathering?”.Finally,we compiledthisdatatoproduceatheoreticalframeworkthatcould supportpotentialcollaborativemanagementarrangements.Pilot interviewsprecededdatacollectiontoreﬁnethesemi-structured questionnaireinJanuaryandFebruary2018.

Thecomprehensiveliteraturereviewwasperformedbyusing “WebofScience”searchengine,followingBogonietal.(2020)and

Monta ño-Centellasetal.(2020).Wesearchedforspecifictermsin theabstractsofarticlespublishedbetween2010and-2020: “arau-caria*”and“angustifolia*”and“conservation*”or“cultural*”.Both terms“conservation”and“cultural”weredefinedbecausetheyare commonlyemployedinscientificpublicationstargetingaraucaria conservationandethnoecologicalstudies.Wefound70scientific peer-reviewedarticles(TableS2)andincludedafewnon-indexed references,suchasPh.D.theses.First,wecross-checkedthe litera-turereviewinformationwithourfieldworkdata.Second,weused

theselectedpeer-reviewedarticlestoproposeaschematic frame-work(TableS3)basedontwoalternativeconservationmodels. Top-downversusbottom-upconservationschemesforthe AraucariaForestSystem

Tocreatethealternativeconservationmodels,wefollowedthe frameworkofcomplexadaptivesystems,whichunderstandsthat social-ecologicalsystemsaredrivenbyexternal factors,suchas policiesandclimatechange,aswellasbyinternalfeedbacks(Berkes etal.,2000;Folkeetal.,2010).Wefirstidentified‘ForestCover’as themainstatevariabledefiningtheecosystemfromthe conserva-tionandamoreholisticperspective.Statevariablesaremeantto representtheoverallstateofasystemandmayindicatethe exis-tenceofalternativestablestates(Folkeetal.2010).Wethendefined twovariablesrepresentingdriversunderatop-downconceptual framework:‘Deforestationandresourceoverexploitation’and‘Forest Protection’.Forthebottom-upconceptualframework,weuseda secondstatevariable‘TraditionalEcologicalKnowledge-TEK’,and ‘Collaborativemanagement’asadriver.Thesevariableswere pre-viouslyidentifiedasthemostimportantforAFSdynamicsinour literaturereviewandrepresentcriticalelementsineach conser-vationmodel (TableS3). For instance,oneof themaingoalsof protectedareasishaltingbiodiversityloss,suchasdeforestation (Rodrigues and Cazalis, 2020).In Brazil, both federal and state governmentsareresponsiblefortop-downconservationmodels, especiallyintheformofProtectedAreas,suchasStrictlyProtected andSustainableUseConservationUnits,orLegalReserves(Metzger etal.,2019; Pachecoet al.,2018).Incontrast,we defined‘TEK’ asanotherstatevariableunderabottom-upconservationmodel becausearaucariacanbeclassifiedasaCulturallyImportantSpecies thatdependon‘TEK’topersist(Adanetal.,2016;Quinteiroetal., 2019;Reisetal.,2014;TagliariandPeroni,2018).Bothconceptual modelssuggestthatalternativefeedbackloopsproducealternative dynamicsofAraucariaForestSystems.Followingthesetwo mod-els,weproposethemainthreats,strategies,andactorsinvolved,as wellasthebenefitsandrisksofbottom-upandtop-down conser-vationstrategies(inspiredbyFreitasetal.,2020).Finally,alsobased onthepublishedliteratureandfielddatafromthisstudythat indi-catesthebottom-upschemeasthemostpromisingformaintaining AFSinthefuture,weevaluatethepossibilitiesforimplementing collaborativemanagementsthatcontributetostrengthening envi-ronmentalgovernanceintheregion.

RESULTS

Socio-economicbeneﬁtsandco-managementpossibilitiesfor araucariaresources

According to our interviews, local smallholders and pinhão extractorsareinvolvedintheextractionofaraucariaseeds (pin-hão),foratleast3.5generations(mean=3.8generations,where eachgenerationrepresents25yearsonaverage).Thereare fam-ilygroupswhohavebeenlivinginthesameregionfor130-150 years(35familygroupsor36%).Thislonginteractionbetweenthe participantswitharaucaria’sresourcesbringslargesocio-economic benefitstolocalfamilies.Amongthe97participants,63(65%)told thatsomehowpinhãotradeinfluencestheirmonthlyincomes,from R$1000toR$2500permonth,i.e.US$490toUS$1235atthetime, in2018(WBI,2020)or∼1to2.3Brazilianminimumwagesin2018. Furthermore,17participantsamongthose63whobenefitedfrom tradeaffirmedthatatleast50%oftheirannualgrossincomecomes frompinhãotrade.Pinhãotradeisamongthethreemainsourcesof incomefor30%ofallparticipants.Livestockandothercropswere commonlycited bysmallholdersas alternativeincome sources, togetherwithpinhãotrade,suchasbeans,corn,yerbamate,and tobacco.Theamountofpinhãogatheredperseasonbythe

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partici-Table1

CollaborativemanagementofAraucariaangustifoliaanditsmainchallengesforimplementation,considering:(i)Implications;(ii)potentialbeneﬁts:cultural, ecological,social-economic,andinstitutionalarrangements,aswellaspotentialrisks;and(iii)theliteraturereviewandinterviews’datatosustainourmodel assumptions(inspiredbyFreitasetal.,2020).Co-managementforaraucariaconsidersmostlytheuse,management,andconsumptionofitsnut-likeseed,although

othermanagementsystemsexist,suchaslegaltimberproduction,reforestation,maintenanceofprivatenativeremnants,andpaymentforenvironmentalservices.We

usedinformationavailableintheliteraturetocharacterizethearaucariaco-managementframework.Here,wedescribeindetailtherisksandbeneﬁtsofthearaucaria

co-management.

Araucariaangustifoliaco-management

Implications Potentialbeneﬁts Reference

Cultural

Participants’engagement(localpeople) Increase Thisstudy(questionsA3;A3a;A7a;B2;B4;seeTableS1)

Communityinvolvement Increase Thisstudy(questionsA3a;A7a;seeTableS1);Adanetal.,

2016

Societalrecognitionandoutreach Increase Freitasetal.,2020

Strengtheningofculturalvaluesand

TraditionalEcologicalKnowledge

Increase Reisetal.,2014;MelloandPeroni,2015;Adanetal.,2016;

TagliariandPeroni2018

Maintenanceofaraucariaethnovarieties Increase Thisstudy(questionsB4;B5;B6;B13;B14b;B14c;B15;

seeTableS1);Adanetal.,2016;TagliariandPeroni2018;

Quinteiroetal.,2019

Ecological

Speciesabundance Increase Thisstudy(questionsA7;A7a;B1;B13;B13b;seeTable

S1);Sühsetal.,2018

AraucariaForestecosystemconservationand

recovery

Increasegeneralresiliencetohuman

andnaturaldisturbances

Folkeetal.,2010

Ecologicalinteractions Increase Bogonietal.,2020

Nut-likeseedproduction Increase Thisstudy(questionsA3;A3a;B2;seeTableS1);Robinson

etal.,2018

Connectivitybetweenaraucaria’sremnant

populations

Maintenanceofaraucariaremnants

throughdifferentProtectedAreas

Tagliarietal.,inreview

Species’geneticdiversity Increase Adanetal.,2016

Contributiontofoodsecurity Increase Thisstudy(questionsA3a;B2.B3;seeTableS1);Reisetal.,

2018

Social-economic

Societalrecognitionandoutreach Increase Reisetal.,2014

Stakeholders’participation Possible Tagliarietal.,2019

Possibilityofﬁnancialself-sustainability Possible Tagliarietal.,2019

Incomedistributionwithinthecommunity Increase Thisstudy(questionsA3;A3a;A7a;seeTableS1)

‘Conservation-by-use’possibility Possible Reisetal.,2018

Historicalcommercialoverpressure Possible Ribeiroetal.,2009;MelloandPeroni,2015;Schneider

etal.,2018

Valueforsustainablearaucariaresourcesuse Possible Tagliarietal.,2019

Opportunitiesforinstitutionalarrangements

Surveillance/enforcement Possiblyincrease Freitasetal.,2020

PaymentforEnvironmentalServicesasa

compensationstrategy

Possible Tagliarietal.,2019

Mainstimulitolocalengagement Cultural/moral/ethicaspects;ﬁnancial

compensation

Thisstudy(questionsA3a;A7a;seeTableS1);Tagliari

etal.,2019

Rulesfocusingonhabitatprotection Increase2 _See_footnote

Legalpermissiontotradethetargetspecies Thereisnolegalpermission3 _See_footnote

Co-managementwiththeconsentof

environmentalagencies(suchastimber

productionquotasforsmallholdersuseand

management)

Possible OrellanaandVanclay,2018

Financialcompensationforsupporting

araucaria’sremnantsbesidesLegalReserves

andPermanentPreservationAreas

Increase Tagliarietal.,2019

Potentialrisks

Reducedinspectionofenvironmentalagencies Possible Freitasetal.,2020

Historicalcommercialoverpressure High Ribeiroetal.,2009;MelloandPeroni,2015;Schneider

etal.,2018

Currentillegalharvestpressure(i.e.

deforestationandlogging)

High Adanetal.,2016;Schneideretal.,2018;Tagliariand Peroni2018;Quinteiroetal.,2019

1_Southern_Brazilian_States_created_their_speciﬁc_laws_for_the_beginnings_of_pinhão_commerce_(i.e._Rio_Grande_do_Sul_starts_from_April₁₅th_;_Santa_Catarina_and_Paraná_from

April1st_)._This_decision_period_is_due_to_the_maintenance_of_local_fauna,_especially_the_parrots_{“Papagaio-charão”}_and_{“Papagaio-do-peito-roxo”}_(Amazona_petrei_and_Amazona

vinacea,respectively),besidessmallrodentsas“cutia”(Dasyproctaazarae),andmammalsas“veado”(Mazamagouazoubira;LobandVieira,2008).Oncetheextractionseason

beginsnolawsregulatetheamountofpinhão(kgortonne)collectedduringtheseasonperiod.

2_Mata_Atlântica_Law_n◦_11.428/2006_–_prohibits_native_species_management_in_natural_forests._CONAMA_Resolution_N◦_278/2001₍_BRASIL,_2006;_CONAMA_-_Conselho_Nacional

doMeioAmbiente,2001).

3_According_to_Brazilian_legislation,_araucaria_native_populations_are_prohibited_for_timber_harvesting_once_the_species_is_{‘Critically}_{Endangered’}₍_Thomas,₂₀₁₃_)._However,

plantedaraucariaharvestingfollowingamanagementplanregisteredandapprovedbyenvironmentalagenciesisallowed,butbureaucracyandlackofﬂexibilityprevent

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pantswasclassiﬁedinthreecategories:(i)upto1000kg(40%or39 participants);(ii)from1000to10,000kg(47.5%or46participants); and(iii)above10,000kg(11.5%or11participants).Formost partic-ipants,however,theextractivismofaraucariaseedsdidnotstand inpracticeaspartofaco-managementscheme,despiteinvolving localmanagementandtrade.Onlyonesmallholderdeclaredthat thepinhãotradeinhisproprietywascertiﬁedbyanNGOunder a co-managementscheme.Thesameparticipantis alsogranted withone projectinvolvingPaymentfor EnvironmentalServices (PES)toconservearaucariaremnantsinareasbeyondtheLegal Reservewithinhisproperty.Fourparticipantsusetheirproperties fortourismpurposesinvolvingaraucaria(i.e.ecotourism).Among thesefourinterviewees,twoofthemhaveco-management part-nerships withinternationalstakeholders and NGOs topromote sustainabletourismintheAraucariaForestregion.

TraditionalEcologicalKnowledgeaboutaraucariamanagement andethnovarieties

Sixty-oneparticipants(63%) saidthat AraucariaForestcover aroundtheproperty(ifapplicable)expandedinthelastdecades dueto:(i)thecreationofProtectedAreas(N=33);(ii)restrictive legislation(N=18),consequentlysawmills’interdictionforusing nativeandthreatenedspecies(N=5);(iii)community participa-tioninreforestation(N=9);and(iv)increaseddispersalbylocal fauna(N=6).Theremaining35participantsinformedthat Arau-cariaForestcoverhasbeendecreasing,mainlydueto:(i)seedling suppression,knownas“roçadas”(N=22);or(ii)illegallogging(N= 18).Wealsofoundintervieweesdescribingnegativeimpactsfrom (iii)pesticides(N=1);(iv)severelegislation(N=1);and(v) eco-logicalcompetitionwithPinussp.(N=1).Weidentified23local namesfortypes(ethnovarieties)basedon320citationsfromall participants.Theseethnovarietiesweredescribedbylocalpeople (i.e.smallholdersand/orpinhãoextractors)accordingtothe ripen-ingperiodsofpinhãoseedsproducedbyfemalearaucarias.Thefive most-cited localvarietieswere: (i)“Macaco”(N=81 citations); (ii)“Cajuvá”(N=80citations);(iii)“Comum”(N=48 citations); (iv)“DoCedo”(N=31 citations);and(v)“25deMarço”(N=16 citations).Mostparticipantscitedthreeethnovarieties(52.5%)and ∼25%ofthemmentionedfourdifferentethnovarieties. Ethnovari-etiesdescribedbytheparticipantsweresaidtodevelopindifferent momentsduringtheyearindicatingpinhãoproductionthroughout theentireyear.

Socio-ecologicalbeneﬁtsandrisksofbothalternativemodelsfor AraucariaForestSystems

Thebenefitsandrisksofadoptinga top-downorbottom-up strategy for Araucaria Forest System involve different ecologi-cal, social, economic, and culturaldimensions according tothe interviewsandtheliteraturereview(Fig.3; Table1).Top-down conservationmodelspromotebenefitstowardsthetargetspecies (inthiscasearaucaria)anditssurroundingfaunaandflora;the bio-diversitymaintenance;andprovidesecosystemservices,suchas provisioning(foodwithpinhãoproduction);support(pollination; nutrient cycling); regulation (carbon sequestration; alternative foodresourceforAraucariaForestfauna);andcultural(heritage value,regionalsymbols,ecotourism).Biodiversityandecosystem servicesmaybeindirectlyenhancedbythismodel,thusfavoring humanwell-being.However,restrictivetop-downmodels(such asStrictlyProtectedareasorexcessiverestrictivelegislation)may create:(i)barriersbetweenhumangroupsandthetarget preser-vationpriority;(ii)thelossofTEKandsocio-ecologicalresilience; (iii)fragilitytoexternalstressors,suchasclimatechange.

Themostpromisingbeneﬁtsofbottom-upco-managementare: (i)sustainablepinhãotrade;(ii)sustainabletourism;(iii)Payment

forEnvironmentalServicesprograms;(iv)potentialconservationof AraucariaForestremnantswithinruralproperties;and(v) possi-blerecoveryandexpansionofAraucariaForests.Byincorporating theseinitiativeswithlocalpeople,theymayalsostimulatelocal engagementinsurveillance,conservation,andmaintenanceof bio-diversity.Thesebeneﬁtsareinterconnectedbetweenlocalgroups andAraucariaForest,enhancingthelong-termresilienceand con-servationof theAraucaria ForestSystem.The risksof adopting bottom-upco-managementschemesforAraucariaForestSystems mayberelatedto:(i)psychologicalbarriersbetweenlocalpeople andenvironmentalagenciesduetothememoryofhistorical exces-siveenforcement–anexampleisapracticeknownas‘roc¸adas’, whichconsistsintheremovalofaraucariajuvenilestoavoidfuture legalrestrictionsonlanduse(Adanetal.,2016)–;(ii)thepotential overexploitationofaraucariaresourceswithinprivateareas,such asillegalcutting,timberexploitation,anddeforestation(Orellana andVanclay,2018);and(iii)possiblepoorcommunicationbetween localpeople, stakeholders, and environmentalagencies (Freitas etal.,2020).However,negativeco-managementexperiencesare morelikelytobecorrectedbypositiveinnovationsfromlocal peo-ples,sincetheirTEKandtheintrinsicbodyofknowledgethrough generations might allow them tomaintain feedbacks stronger, respondingfastertoexternalchanges,enhancingadaptability,and transformabilityofthesystem(asshownbyBerkesetal.,2000).

TwoalternativemodelsofAraucariaForestconservation: top-downwithrestrictiveuse,andbottom-upwith co-managementschemes

TwoalternativeconservationmodelsofAraucariaSESshowed different feedbacks and dynamics (Fig. 4; Table S3). The top-downrestrictiveschemecontributedtoincreasingforestresilience tohumandisturbances.Thishappensbecause‘deforestation’and ‘resource overexploitation’ lead to more enforcement and ‘forest protection’(restrictive measures) by managerstomaintain ‘for-est cover’. With more forest cover, resource overexploitation is expected to decrease, relative to the overall forest abundance, reducing theperceptions of overexploitationby managers, and leadingtolessrestrictivemeasures.Inthissense,weidentiﬁedthat restrictivemeasuresarecreatedasaresponsetohuman distur-bances(i.e.deforestationorresourceoverexploitation),resultingin anegativefeedbackloopthatdampensforestloss(seeFig.4)and partlymaintainstheconservationpurpose.Thetop-downscheme, however,mightnotguaranteeresiliencefortheentiresystemto othertypesofdisturbances,suchasextremeweathereventsdue toclimatechange,mainlybecausethelossoftraditional manage-mentmayreducethefunctionaldiversityofaraucariapopulations (Table1;Adanetal.,2016),andconsequentlytheforests’ adap-tivecapacity in the face of unexpectedevents (Elmqvist et al., 2003).Hence,thetop-downschemecompletelydisruptsthe his-toricalhuman-plantinteractionoftheAFSthatmadethissystem resilient for millennia. In contrast, thebottom-up conservation schemeshoweda distinctfeedback loop(Fig.4).Inthis case, a self-reinforcing(positive)feedbackloopemerged inthesystem, because‘TraditionalEcologicalKnowledge (TEK)’provides oppor-tunitiesfor‘collaborativemanagement’,whichallows‘forestcover’ topersistand potentially expand.With more forestcover, TEK is expectedtoexpand as well,promoting co-managementthat enhancesthegeneralecologicalresilienceoftheforest(toallsorts ofunexpecteddisturbances),becauselocalmanagementenhances thefunctionaldiversityof araucariapopulations(Table1;Adan etal.,2016).Thepositivefeedbackloopweidentiﬁedhastherefore thepotentialtostrengthentheecologicalresilienceofthewhole AraucariaSESandtopromotethesystem’sexpansionbeyondits currentlimits.

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Fig.3.Flowchartofbeneﬁtsandrisks(inspiredbyFreitasetal.,2020)ofdistinctconservationstrategies.Arrowsrepresenttheexpectedoutcomesofeverystepinthe

ﬂowcharts.1.Top-downstrategiesforAraucariaangustifolia(araucaria)preservation.Asthemainconservationstrategy,top-downpolicies,suchasthemaintenance

orcreationofStrictlyProtected,neglectthehistoricalhuman-plantinteractionintheAraucariaForestSystem.Thesepolicies(1)maintaintheecologicalresilienceofthe

forestecosystemandprovideecosystemservices(indirectbeneﬁtsforhumangroups),but(2)mayfailduetobarriersupontraditionalpeoplewhouse,manage,and

promotethesocio-ecologicalresilienceofthesystem,leadingtothelossofTEK;increasesinoverexploitationanddeforestationpressures;andreducedresiliencetoexternal

stressors,suchasclimatechange,pathogens,andinvasivespecies.2.Bottom-upconservationinitiativesforaraucariaasaCulturalImportantSpecies(CIS)under

co-management.Becausearaucariaisaculturallyimportantspeciesforlocalpeople,(1)theywilllikelyfeelstimulatedtoengageinco-managementinitiativesfocusingonthis

species;(2)weshouldconsequentlyexpecthighcomplianceandlocalsurveillancelocalpeople;(3)thishuman-plantinteractionwhichwilllikelyfavortheconservation

ofaraucariapopulationsand(4)beneﬁtotherspeciesco-existingintheAraucariaForest,andtheecosystemasawhole.Therearebothbeneﬁtsandrisksthatcouldbe

expectedfromthisco-managementapproach.Therisks(5)ofthisinitiativemayberelatedtothepotentialfragilearrangementbetweenlocalpeopleandinstitutions

(e.g.environmentalagencies,Non-GovernmentalOrganizations,privatesectorand/orstakeholders);inadequatesurveillanceoftheco-managementinitiative;and/orthe

excessiveinstitutionalenforcement.Anotherriskistheincreaseofillegalcutting(i.e.resources’overexploitation,juveniles’suppression,and/ornon-sustainabletimber

production).Suchnegativeconsequences(6)willpossiblyaffectecological(i.e.ecosystemdegradation),economic(i.e.lesspinhãotrade,lossofpaymentsorcompensations

forenvironmentalservices;lessecotourism),andcultural(detachmentfromlocalpeople,lossoftraditionalknowledge)aspects.Apotentialwaytocircumventthoseproblems

(e.g.increaseddeforestation)couldbe(7)alternativeco-managementinitiativestargetingforestrecoveryorrecuperationofdegradedareas(dashedarrow).Thepositive

scenario(8),however,couldbringecological(maintenanceoftheecosystem);economic(viaPaymentforEnvironmentalServices,sustainablepinhãotrade,ecotourism);social

andculturalbeneﬁts(i.e.localengagement;maintenanceoftheTraditionalEcologicalKnowledgeofaraucariaanditsethnovarieties,andaraucariaresources’management).

Allofthesepositiveconsequencesareinterconnected(9)andcouldﬁnallyallowamoreresilientandcyclicalstablestate(10)oftheentireeco-socio-economicsystemof

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Fig.4. Theschematictop-downandbottom-upconservationmodelsofAraucaria

Forestsystemsareself-organizedincontrastingways,withdifferentfeedbacks.

Solidlinesrepresentpositive/negativeeffects.Cycleschemes(grayshaded)

rep-resent thefeedback loop,itsdirection (i.e.counter-clockwise) andits result:

negative/buffereffectorpositive/self-reinforcingstate.1.Schematic

representa-tionoftheinteractionsinvolvedintop-downpolicies,suchasStrictlyProtected Areas.Thisschemeimprovesonlyaportionofthetargetecosystem,neglecting

potentialsocio-ecologicalinteractions(i.e.localpeople).Thisclassical

conserva-tionistapproachcreatesabufferfeedback,i.e.itsustainsthecurrentstate.Excessive

resourceexploitationordeforestationgeneratesprotectivemeasuresthatbeneﬁt

forestcover.However,aforestprotectedbytop-downmeasuresmaynotcompletely

avoidthesedisturbances(e.g.deforestationandoverexploitation)andmightnot

contributetootherexternalstressors,suchasclimatechange.Theyalsoreducethe

beneﬁtsforlocalpeoples,whoarevirtuallyexcludedfromthesystem.2.Schematic

representationoftheinteractionsproducedbybottom-uppolicies.

Indepen-dentlyfromrestrictivemeasures,thisschematicsocio-ecologicalsystemindicates

anincreaseinthesystem’sresilience,duetoaself-reinforcingmechanismthat

pro-motesaraucariaforestexpansion.Hence,byincorporatingTEKandco-management

initiatives,thisschemeincreasesthegeneralresilienceofthesocial-ecological

sys-tem.Note:ourconceptualmodelisnotmutuallyexclusive,bothtop-downand

bottom-upstrategiesco-occurwithinAFSandcontributetomaintainingnative

forestremnants.

DISCUSSION

OurﬁndingsrevealthatAraucariaForestSystemsinsouthern SouthAmericamightbelosingresilienceduetoalong-term top-downrestrictivemanagementschemethatmakesthesystemless adapted toall sortsof disturbances. Partly becausethis social-ecologicalsystemdependsonTEK,whichiscurrentlybeinglost as restrictive measuresdisrupt anancient human-nature inter-action.However,ourstudyrevealsanalternativeperspectiveon howtomaintainthegeneralresilienceofAraucariaForestSystems bystimulatingTEKproduction throughacollaborative manage-ment scheme.Wehave shownthat bottom-upco-management mayself-reinforceandbeneﬁttheresilienceofaraucariaforestsand thusprovideapossiblesolutionfortheconservationdilemmathat hasbeenthreateningthisecosystem.Co-managementinitiatives mayeffectivelyincorporatetheprinciplesofresilience-thinking: management of feedbacks;maintenance of ecologicaldiversity; and broad participation of different actors (Folke et al., 2005,

2010).Strengtheninglocalactorsandtheirrolesingovernanceis

particularlyeffectivewhencomparedtorestrictiveand exclusion-aryconservationstrategies,suchasStrictlyProtectedAreaswith excessivetop-downenforcement.Webelieveourfindingsofferan opportunitytogenerateoptimisticbottom-uppathwaystowards anefficient,inclusive,andwell-articulatedconservationstrategy thatcouldself-reinforcestheresilienceoftheAraucariaForest Sys-tem.Byshiftingfromatop-downtoabottom-upco-management schemethatincludeslocalactorstogetherwithexistinginstitutions inthegovernanceprocess,theAFScoulddeveloptransformability andadaptability,furtherenhancingitssocial-ecologicalresilience (seeFolkeetal.,2005,2010;Biggsetal.,2012;Bennetetal.,2016). Becausesimilarecosystemswithculturallyimportantplantspecies arealsoundergoingthesameconservationdilemma,webelieve thatourfindingscouldbeusefulinothercontexts.Such innova-tiveandcollaborativesystemscouldpotentiallydeveloptobecome anotherglobalbrightspotexample,wherethenaturalandcultural capitalsarepreservedbybottom-uparrangements,inspiring soci-etiesworldwide(Bennettetal.,2016).

Althoughthetop-downstrategyhasprovenusefultomaintain araucaria forestsresilient to logging and other human degrad-ingactivitiesviaa negativefeedbackloop(Fig.4), this strategy hasnotbeensufﬁcienttomaintaintheentiresysteminthelong run.Sincethehistoricalloggingoverexploitationinthe19th

cen-tury,andlater,theinclusionofaraucariaas“CriticallyEndangered” byIUCN(Thomasetal.,2013),thecreation/maintenanceof top-downProtectedAreasbecamethecornerstoneofitsconservation (Zechinietal.2018).ProtectedAreasaimtocurbanthropogenic disturbancesinnaturalecosystemsandhaltthelossofbiodiversity (Geldmannetal.,2019;Wiensetal.,2011),butmightfailtoprevent theextinctionofseveralspeciesinthelong-termduetoclimate change(Ferroetal.,2014),aswelltoanthropogenicdisturbances (e.g.,invasivespecies;poaching;landuse;lossofgeneticdiversity;

Laurance,2013);andtopotentiallypromotesocio-economic bene-ﬁts(givenpoorgovernanceorregionalconﬂicts;Lauranceetal., 2012).Insouthern Brazil,traditionallandmanagement systems protectthegeneticdiversityofaraucariapopulations,thus con-tributingtothespeciesconservationandthesafeguardingofthe SES(Reisetal.,2014;MelloandPeroni,2015;Adanetal.,2016;

Zechinietal.,2018).Asaresult,top-downconservationstrategies areinsufﬁcienttoconserveaculturallandscape(MelloandPeroni, 2015)becauseitreducesthesystems’adaptivecapacity,aswellas theparticipationofdifferentactorsinenvironmentalgovernance; allrequisitesforsocial-ecologicalresilience(Folkeetal.,2010;de Vosetal.,2016;Musavengane,2019).

Thefeedbackdynamicsofabottom-upco-management strat-egyhasthepotentialtoenhancethesystemic resilienceofAFS aswellasother Social-EcologicalSystems,becauseit promotes adaptability through TEK production (Berkes et al., 2000), and becauseitrecognizesthattransformabilityintoparticipatory gov-ernance is necessary, as human-nature has shaped Araucaria Forest landscapes over millennia (Reiset al., 2014).Moreover, itenhancesconnectivity,becausedifferentactorsareconnected in the system (e.g. NGOs; stakeholders; local groups; govern-ments).Also,itretainsfunctionalredundancy,i.e.ifoneactoris removedfromthesystemthesystemitselfremains resilientto thedisturbancebecauseofthe differentplayerswiththesame functions.We alsofoundsupportforthenotionthata bottom-upco-managementstrategycanenhancetheresilienceofAFSnot onlytohumandisturbancesbutalsotodifferentkindsofthreats, suchasextremeweatherevents(Folkeetal.,2010).Onereasonis thatco-managementincreasesthefunctionaldiversityofaraucaria treepopulations,especially due touseand management (Adan etal.,2016;TagliariandPeroni,2018;Quinteiroetal.,2019),and consequentlytheadaptive capacity oftheforest tounexpected disturbances(Elmqvistetal.,2003).Asaresult,co-management generatesapositivefeedbackloopthatstrengthensforestresilience

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aswellassocioculturalresilience.TheAraucariaForestisan exam-pleofa self-reinforcingsystem,where inthepasthuman-plant interaction wasresponsiblefor theforestexpansionbeyondits climaticniche(Robinsonetal.,2018).

Sühs etal.(2018)showedthatthemaintenance ofaraucaria maturetreestogetherwithtraditionallandmanagementpromotes Araucaria Forest expansion, saplingspecies richness and abun-dance,togetherwiththepreservation ofgrasslandsinsouthern Brazil.Theauthorsarguethatamaximalregionaldiversityofthe plant communitiescan beachieved bya balancebetween pre-servedforest areasandtraditional managementpractices (Sühs etal.,2018).Reisetal.(2018)alsoshowedthatmanagement sys-temswithintheAraucariaForest,suchasthe“caívas”and“faxinais”, maintainlandscapeswithproductiveforestfragments,thus favor-ingaraucaria conservationandhumanwell-being.Furthermore, thissystemhighlydependsontheculturalandeconomic valua-tionofpinhão(Reisetal.,2018).Theopportunitytoincreaseproﬁts fromaraucariaremnantscouldassurethelong-term sustainabil-ityofco-managementinitiatives(PomeroyandBerkes,1997).The broaderparticipationofdifferentactorsinenvironmental gover-nanceiswithinthebasisofco-managementinitiatives(seeFreitas etal.,2020).Hence,co-managementinitiativestargetingthe Arau-cariaangustifoliacanrepresentavaluablesolutionfortheongoing conservationdilemma.

CONCLUSION

Re-evaluatingthearaucariaconservationdilemma

Ourbottom-upconceptualmodelwasdirectlylinkedtoa spe-ciﬁc socialgroup:thesmallholdersalongtheAFS,whopossibly encompassthemajorityofAFSnativeremnantsundertheirLegal Reservesprotectedareas(BittencourtandSebbenn,2009;Metzger etal.,2019).Othersocialgroupsstillinﬂuenceandmanagethis sys-tem,suchasindigenouspeoples,whowereco-responsibleforthe transformationandexpansionofthesysteminthepast(Robinson et al., 2018), and remain as essential partners for developing a co-management scheme. Although we could not incorporate indigenous peoples inouranalysis,theyalsoapplytoour con-ceptualmodelasmajorTEKholders.Itisimportanttorecognize that theAFSis alsocomposedof amosaic oflandowners, agri-culturalenterprises,timberandcellulosecompanies,wherenative remnantsarestillprotectedbytop-downmanagement,suchasin StrictlyProtectionConservationUnitsandLegalReserves. There-fore,ourconceptualmodelsarenotmutuallyexclusive,andboth top-downandbottom-upstrategiesmayco-occurwithinAFSand contributetomaintainingnativeforestremnantsresilientinthe faceofglobalchanges.

AraucariaForestSystemsareaheritage,leftbypastindigenous societiesthatoncelivedintheregion(Reisetal.,2014;Robinson et al.,2018),and thatnow representsa valuable assetfor local humanpopulations (Melloand Peroni,2015;Adanetal., 2016;

TagliariandPeroni,2018;Quinteiroetal.,2019).Ourﬁndings indi-catethatthisheritagemightbeatriskinthelong-termforfuture generations.Thecollaborativemanagementstrategybetweenlocal peoples and otherinstitutionsinterestedin theconservation of theseancientandendemicforestsisnecessaryasanalternative strategytomaintainthissocio-ecologicalsystem.However,legal aspectsmayremovelocalpeoplefromdecision-makingand poten-tiallyproduceantagonisticactionsduetorestrictiveconservation measures,suchasseedlingsuppression(Adanetal.,2016;Tagliari andPeroni2018;Quinteiroetal.,2019)ortimberillegal exploita-tion(Schneideretal.,2018).Thisproblematicmayengenderwhat isknownasthe‘EnvironmentalPsychologicBarrier’,wherelocal peopletend toavoid effectiveactiontoimprove/conserve their

surroundingenvironment,eveniftheyperceivethattheseactions bringbiodiversitylossesandnegativeimpactstotheirlives,such aslossoflifequalityandfoodsecurity(TamandChan,2017).Still, otherco-managementinitiativesofculturallyimportantspeciesin Brazilshowedpositiveoutcomesbymaintainingtheplant-human interaction,suchasthoseinvolvingHeveabrasiliensisand Berthol-letiaexcelsa(“rubbertree”and“Brazilnuttree”,respectively)inthe BrazilianAmazon,andRumohraadiantiformis(“samambaia-preta”) in southern Brazil (De Souzaet al., 2006; Gomes et al., 2018). Co-managementprogramswiththesespecieslargelycontributed tomaintainingtheeconomiclivelihoodsandTraditional Ecolog-icalKnowledgeoflocalsmallholdersandpeoplefromindigenous andlocalcommunities(e.g.indigenouspeople,“ribeirinhos”,and/or “caic¸aras”;De Souzaetal.,2006;Gomes etal.,2018).Similarly, theconservationoftheAraucariaForestSystemdependson main-tainingTEKandpromotingcollaborativemanagementinitiatives, becausebottom-upconservationstrategiesaremorelikelyto pro-ducethetransformationsthatthesystemneedstopersistinthe uncertainfuture.Byincorporatingallactorsofthissocio-ecological system,resilienceisreinforcedtowardsexpansion,maintenanceof TEK,andparticipatorysystemicsocio-ecologicalconservation.

CONFLICTOFINTEREST

Theauthorsdeclarenoconﬂictofinterest.

AUTHOR’SCONTRIBUTION

MMTconceivedthemainidea,draftedthemanuscript,analyzed interviews’data,anddidthemainliteraturereview.GDBdrafted themanuscriptanddidtheliteraturereview.CLcontributedtothe literaturereviewanddevelopedthemainstructureofthearticle. BFbroughtvaluableinsightsthattransformedthepurposeofthis study.CFreviewedtheearlyversions,suggestedmainchangesin thestructureofthemanuscript.JBcontributedtothedraft evalua-tion,improvedtheinterviewquestions,andanalyzedthedata.GV contributedwiththeearlyversionsofthemanuscriptandinsights aboutpotentialknowledge-gaps.NPcontributedtodraft develop-ment,literaturereview,insightsaboutknowledge-gaps,improved theinterviewquestions,reviewedtheearlyversions,andproject ﬁnancing.Allauthorscontributedcriticallytothedraftsandgave ﬁnalapprovalforpublication.

DATAAVAILABILITYSTATEMENT

ThismanuscriptispartofanongoingPh.D.thesis.The infor-mationgatheredintheethnoecologicalsurveyswillnotbeableto shareuntilthepublicationofanotherspeciﬁcchapter.However, asamanuscriptbasedontheliteraturereview(alreadypublished elsewhere)andcomplementedwiththeethnoecological informa-tionusedinthequestionnaire(seedetailsinSupplementaryFile TablesS1,S2,S3),thereadersmayﬁndthecoreinformationused inthismanuscript.

ACKNOWLEDGMENTS

MMTthanksalllocalpeopleinterviewed between2018and 2019 who contributed with their knowledge about araucaria, theculturallandscape, and thechallenges smallholders face in Brazil. The authors would like to thank the Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nível Superior (CAPES/Brazil; Finance Code 001) for the Ph.D. scholarship for MMT and GDB. CL thanks CAPES for the post-doctoral fellowship (no

88887.474568/2020).NPthanksCNPqfortheproductivity scholar-ship(Process310443/2015-6).CTFthankstheFundac¸ãodeAmparo

(11)

àPesquisadoEstadodeSãoPaulo(FAPESP)forthepost-doctoral fellowship (Process no 2019/15550-2). JAB is supported by the SãoPauloResearchFoundation(FAPESP)postdoctoralfellowship grants2018-05970-1and2019-11901-5.Thisstudyisdedicatedto EstelamarisandPatrick.

AppendixA. Supplementarydata

Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/ j.pecon.2021.03.002.

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