Edge disturbance drives liana abundance increase and ... Campbell...tion of forest succession, and a substantial decline in forest carbon storage. We ex-amined the individual impacts

Ecology and Evolution 201884237ndash4251 emsp|emsp4237wwwecolevolorg

Received29September2017emsp |emsp Revised26January2018emsp |emsp Accepted9February2018DOI 101002ece33959

O R I G I N A L R E S E A R C H

Edge disturbance drives liana abundance increase and alteration of lianandashhost tree interactions in tropical forest fragments

Mason J Campbell1 emsp|emspWill Edwards1emsp|emspAinhoa Magrach23emsp|emsp Mohammed Alamgir1emsp|emspGabriel Porolak1emsp|emspD Mohandass4emsp|emspWilliam F Laurance1

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsEcology and EvolutionpublishedbyJohnWileyampSonsLtd

1CentreforTropicalEnvironmentalandSustainabilityScience(TESS)CollegeofScienceandEngineeringJamesCookUniversityCairnsQueenslandAustralia2BasqueCentreforClimateChange-BC3LeioaSpain3EstacioacutenBioloacutegicadeDontildeana(EBD-CSIC)SevillaSpain4RootandSoilBiologyLabDepartmentofBotanyBharathiarUniversityCoimbatoreIndia

CorrespondenceMasonJCampbellCentreforTropicalEnvironmentalandSustainabilityScience(TESS)CollegeofScienceandEngineeringJamesCookUniversityCairnsQueenslandAustraliaEmailmasoncampbell1jcueduau

Funding informationCowanBursaryBasqueGovernmentAustralianLaureateFellowshipAustralianResearchCouncilDiscovery

AbstractClosed-canopy forests are being rapidly fragmented across much of the tropicalworldDetermining the impactsof fragmentationonecologicalprocessesenablesbetterforestmanagementandimprovesspecies-conservationoutcomesLianasareanintegralpartoftropicalforestsbutcanhavedetrimentalandpotentiallycomplexinteractionswiththeirhosttreesTheseeffectscanincludereducedtreegrowthandfecundityelevatedtreemortalityalterationsintree-speciescompositiondegrada-tionofforestsuccessionandasubstantialdeclineinforestcarbonstorageWeex-aminedtheindividualimpactsoffragmentationandedgeeffects(0ndash100-mtransectfromedgetoforestinterior)onthelianacommunityandlianandashhosttreeinteractionsin rainforestsof theAthertonTableland innorthQueenslandAustraliaWecom-paredthelianaandtreecommunitythetraitsofliana-infestedtreesanddetermi-nantsoftheratesoftreeinfestationwithinfiveforestfragments(23ndash58hainarea)and five nearby intact-forest sites Fragmented forests experienced considerabledisturbance-induceddegradationattheiredgesresultinginasignificantincreaseinlianaabundanceThiseffectpenetratedtosignificantlygreaterdepthsinforestfrag-ments than in intact forestsThecompositionof the lianacommunity in termsofclimbingguildswas significantlydifferentbetween fragmentedand intact forestslikelybecauseforestedgeshadmoresmall-sizedtreesfavoringparticularlianaguildswhichpreferentiallyusetheseforclimbingtrellisesSitesthathadhigherlianaabun-dancesalsoexhibitedhigherinfestationratesoftreesasdidsiteswiththelargestlia-nasHowever large lianaswere associatedwith low-disturbance forest sitesOurstudyshowsthatedgedisturbanceofforestfragmentssignificantlyalteredtheabun-danceandcommunitycompositionoflianasandtheirecologicalrelationshipswithtreeswithlianaimpactsontreesbeingelevatedinfragmentsrelativetointactfor-estsConsequentlyeffectivecontroloflianasinforestfragmentsrequiresmanage-mentpracticeswhichdirectlyfocusonminimizingforestedgedisturbance

K E Y W O R D S

climbingguildcompetitiondisturbancefragmentationinfestationmanagementvine

4238emsp |emsp emspensp CAMPBELL Et AL

1emsp |emspINTRODUC TION

Habitat fragmentation is globally ubiquitous (Bhagwat 2014RiittersWickhamCostanzaampVogt2016WadeRiittersWickhamamp Jones 2003) In fact it is currently estimated that 70 of theworldrsquosremainingforestiswithin1kmfromaforestedge(Haddadetal2015)This is importantasthefragmentationofforestsandassociatededgeeffectscanreducebiodiversityanddegradeforestfunctioning (eg Fahrig 2003 Laurance Delamonica LauranceVasconcelosampLovejoy2000Lauranceetal20022011MagrachLaurance Larrinaga amp Santamaria 2014a Saunders Hobbs ampMargules1991)Forinstanceforestfragments(32m2ndash100ha)areestimatedtopossess13ndash75lessdiversitythancomparablenon-fragmented forests (Haddad etal 2015)with themajority of thelostdiversityoftenthemost iconiccomponentssuchasbig treesandlargemammals(Chiarello1999Gibsonetal2013Laurance1997bLauranceetal2000OliveiraSantosampTabarelli2008)Inadditionforestfragmentationisalsoknowntoalterordegrademanybeneficialecologicalprocessessuchaspollinationandseeddisper-sal(CampbellLauranceampMagrach2015aCampbellMagrachampLaurance2015bLauranceetal2002Magrachetal2014aPehLinLukeFosterampTurner2014Terborghetal2001)

In the tropics large-scale deforestation has resulted in forestfragmentsnowrepresentingasubstantialproportionoftheremain-ingforestedareainmanyregionssuchastheAtlanticforestofBrazilWestAfricaandtheAthertonTablelandofnortheasternAustralia(Ouedraogo etal 2011 RibeiroMetzgerMartensen Ponzoni ampHirota2009WinterBellampPahl1987)Insuchregionsforestfrag-mentsprovide theprimaryorsole repository for thepreservationofmany rare andendangered species and threatenedecosystems(Arroyo-RodriguezampMandujano2006Arroyo-RodriguezPinedaEscobarampBenitez-Malvido2009Guindon1996)Maximizingtheconservationvalueofforestfragmentsrequiresthatfragmentsarenotonlyretainedbutaremanagedeffectivelywhichnecessitatesanunderstandingoftheirinternalecology

Oneofthemajorecological interactionsalteredbyfragmenta-tion is therelationshipbetweentreesand lianasLianasdetrimen-tally impact trees by limiting seedling recruitment (Schnitzer ampCarson2010SchnitzerDallingampCarson2000)damagingsaplingsanddecreasingtreegrowthandfecundity(Stevens1987)compet-ingwith trees for limited resources (PasquiniWrightamp Santiago2015ReidSchnitzerampPowers2015Rodriacuteguez-RonderosBohrerSanchez-Azofeifa Powers amp Schnitzer 2016 Schnitzer Kuzeeamp Bongers 2005) and increasing tree mortality (IngwellWrightBecklundHubbellampSchnitzer2010)Inadditionlianascanmod-ify the functioning of a forest by reducing carbon storage capac-ity (DuraacutenampGianoli 2013 vanderHeijden Schnitzer PowersampPhillips 2013 Schnitzer van der Heijden Mascaro amp Carson2014) re-distributing nutrients (Kazda 2015 Powers Kalicin ampNewman 2004 SchnitzerampBongers 2011) altering tree-speciescomposition (ClarkampClark1990Lauranceetal2001SchnitzerampBongers2002)threateningepiphyticferns(MagrachRodriacuteguez-PeacuterezCampbellampLaurance2014b)and limitingorchanging the

trajectoryoftree-speciessuccessionwithintreefallgaps(SchnitzerampBongers2005SchnitzerampCarson20012010Schnitzeretal2000)Thus lianascanhavesignificant impactsonboth thebiotaand functioning of remnant forest fragments Understanding theecological interactionsbetween lianasandtheirhost trees iscriti-cal forsuccessfullymanagingremnantforestfragmentsespeciallythosewithhighconservationvalue

There is strong support for theobservation that lianasprefer-entially impact certain ecological ldquoguildsrdquo of tree species such aslate-successionalclimax species (Campbell etal 2015a 2015bClarkampClark1990 Lauranceetal 2001 Schnitzer etal 2000)althoughthereislittleevidencethatthisoccursataspecies-specificlevel (Garrido-Perez amp Burnham 2010 Hegarty 1991 Peacuterez-SalicrupSorkampPutz2001)Theenhanced liana infestationrateson late-successional treespecies is likelyduetotheadvancedage(andthustimeavailableforpossibleinfestation)ofthesetreesandcertain character traits they possess (Hegarty 1991 Schnitzer ampBongers2002)Suchtraitsincludebarkmorphologyandchemicalcomposition (BoomampMori1982Carsten JuolaMaleampCherry2002vanderHeijdenHealeyampPhillips2008Putz1980TalleySetzer amp Jackes 1996) buttresses (Black amp Harper 1979 BoomampMori 1982 Putz 1980) leaf shedding and leaf and stem flexi-bility (Maier 1982 Putz 1984a Rich Lum Munoz amp Quesada1987) treetrellis diameter (ClarkampClark 1990 Perez-SalicrupampdeMeijere2005Peacuterez-Salicrupetal2001Putz1984b) spines(Maier1982Putz1984aRichetal1987)lianandashhostdistanceandavailability (Arroyo-Rodriguez amp Toledo-Aceves 2009 Campbelletal 2017 Muthuramkumar etal 2006 Roeder Slik HarrisonPaudel amp Tomlinson 2015) and synergisms among these traits(SfairRochelleRezendeampMartins2016)Assuchacomparativeassessmentofthepredominanttreetraitsbetweenintactandfrag-mentedforestsandtheirassociationwithlianainfestationmaybeofuseas aproxy todeterminehow forest fragmentation impactslianandashtreeinteractionsandcontributestoincreasedlianaabundancewithinfragmentedforests(Lauranceetal2001)

Thetotalabundanceof lianasisknowntobepositivelyasso-ciatedwithforestedgesandareasofdisturbance(Lauranceetal2001 2014b Ledo amp Schnitzer 2014 Magrach etal 2014bMohandass Campbell Hughes Mammides amp Davidar 2017Mohandass Hughes Campbell amp Davidar 2014 Putz 1984b)High lianaabundancesat forestedgesare likelydue toedgeef-fects (eg Harper etal 2005 Laurance etal 2002 Magnagoetal 2016 Murcia 1995 Williams-Linera 1990) in particularto the increased availability of climbing trellises (ie smaller-stemmedtreesBalfourampBond1993ChittibabuampParthasarathy2001 Londre amp Schnitzer 2006 Putz 1984b Williams-Linera1990)Moreoverforestedgesareoftenmoredisturbedthanfor-estinteriors(Lauranceetal199720112018MagnagoRochaMeyerMartinsampMeira-Neto2015)resultinginincreaseddesic-cationandlightlevelsTheseconditionspreferentiallyfavorlianasover trees throughmechanisms suchasdifferential recruitmentsuccess and resource-interception capacity (Andrade MeinzerGoldsteinampSchnitzer2005Chenetal2015LedoampSchnitzer

emspensp emsp | emsp4239CAMPBELL Et AL

2014OliveiradeMelloampScolforo1997Perez-SalicrupampBarker2000 Rodriacuteguez-Ronderos etal 2016 Schnitzer amp Carson2010)Consequently it is important thatanystudyof lianandashtreeinteractions examine the spatial distributionof lianas in relationtoforestedges

Analyzing the abundance of lianas within climbing guilds be-tween intact and fragmented forests can also be used to assesslianandashhosttreeinteractionsForexampleassessingtheproportionoflianaswithinclimbingguildscanrevealthecurrenttrellisavailabil-ityandthusthesuccessionalstateoftheforest(HegartyampCaballe1991Lauranceetal2001Mohandassetal2014Putz1984b)This ispossiblebecause lianaswithindifferentclimbingguildsuti-lize trellisesof differingmaximal diameter (BalfourampBond1993Putz1984b1990PutzampChai1987)For instanceclimbersthatattachwithadhesiverootsarenotlimitedbytrellis(ietreebranchor trunk)sizewhereasmainstemtwiningandbranchclimbersuselargertrellises(branches)thandotendrilandhookclimbers(BalfourampBond1993Putz1984b1990PutzampChai1987)

Herewecompare the responseof lianas to forest fragmenta-tion edge effects and lianandashhost tree interactions in fragmentedand intactforestswithintheheavilyfragmented landscapeoftheAthertonTablelandinnortheasternAustraliaInthisstudyweaimedtodeterminewhetherforestfragmentationaltersthelianacommu-nityonforestedgesandifsowhetherthisispredominantlydrivenbylandscapelevelfragmentationimpactsorthoseatasmallerhab-itat(iewithinpatch)spatialscaleTodetermine(i)theseparatein-fluenceoffragmentationandedgeeffectsonlianaabundancetreeinfestation rates and liana size (diameter at breast height [DBH])we askedwhatwere the important environmental and ecologicalpredictors associated with thesemeasures at the landscape level(in fragmented and intact forests) and are these similarWe hy-pothesized that liana abundance and tree infestation rateswouldbe greater on fragmented forest edges given the higher rates ofdisturbance they are known to experience (Laurance etal 2018)asdisturbance is aprimarydriverof lianaabundance (SchnitzerampBongers2002)Secondweassessedhabitatscaletraitsbyasking(ii)dotreemorphologicaltraits (treebarktypeorbuttressing)and

treelocationwithrespecttotheforestedgeinfluencelianainfesta-tionrateswithinfragmentedandintactforestsandifsoarethesein-fluencessimilarbetweenthesetwoforesttypesWehypothesizedthatlianaabundanceandtreeinfestationrateswouldbegreateronsmaller-sizedtreesandthosewithroughbarkgiventhatthesetraitscanfacilitatecolonizationbylianasAgainwealsohypothesizedthattreeson fragmented forestedgeswouldexperiencegreater levelsof infestationthanthoseof intact forestsgiventhe increaseddis-turbanceinthoselocations(andthussmalltreetrellissize)andthatthesevariableswouldhaveanegativerelationshipwithdistancetoforestedgeFinallytodeterminetheresponseofthelianacommu-nity to forest fragmentationandedgeeffectsweasked (iii) doesthelianacommunityclimbing-guildcompositionvarybyforesttype(fragmentedor intact) and is this relationship affectedby thedis-tancetotheforestedgeWehypothesizedthatlianaguildsutilizingsmaller-sizedtrelliseswouldincreasedisproportionately(whencom-paredtootherclimbingguilds) infragmentedforestsandclosertoforestedgesduetotheincreasedavailabilityofsmallertrellisesattheselocations

2emsp |emspMATERIAL S AND METHODS

21emsp|emspStudy area

Our study was located on the Atherton Tableland northeasternQueenslandAustralia(Figure1a)TheAthertonTablelandisanup-landhillyplateauranginginelevationfrom~600to1100mMeanannualprecipitationoftheAthertonTablelandsrangesfrom1400to3000mmduetoalocalizednorthwest(low)tosoutheast(high)rainfall gradient however the variation in the study area ismuchless (~200mm) Most annual rainfall occurs during a pronouncedwetseasonfromJanuarytoAprilTheareaisalsopronetocyclonicepisodesduringthewetseason(Turton2012)whichcanresultinin-creasedprecipitationandforestdisturbance(TurtonampSiegenthaler2004TurtonampStork2009)

Thelocalvegetationofthestudyareaisremnantfragmentsandregrowthofalargerrainforestexpansethatpreviouslycoveredthe

F I G U R E 1emsp (a)LocationofthetenstudysitesontheAthertonTablelandsAustraliaStudysitesareindicatedastrianglesforintactforestsandcirclesforfragmentedforestMalandaasthenearesttownisindicatedwithanasterisk(b)thedesignofvegetationsamplingateachstudysitewhereinfive20times20mplotswerestratifiedandrandomlyplacedwithrespecttotheforestedge


Atherton Tableland now isolated by a predominantly agriculturalland-use matrix (Figure1a) Deforestation of this area has beenextensivewithover76000hacleared forcattlepastureandcroplands (Winter etal 1987) Additionallymost of the remnant rainforestvegetationhasbeenselectivelyloggedforvaluablehardwoodtimberspeciessuchasRedCedar(Toona ciliata)(EachamHistoricalSociety19791995Pearson2008)Neverthelessmanyof theseforestfragmentsformalargepartofthegreaterWetTropicsWorldHeritagearea(UNESCO1988)

The remnant vegetation of the area is described as complexmesophyll vine forest and notophyll vine forest with drier areastransitioning into complex semievergreen notophyll vine forest(QueenslandHerbarium 2015 Tracey 1982)Within the complexmesophyllvineforestmultipleintactcanopiesmaybepresentwiththe upper canopy averaging a height of 20ndash40m and emergenttrees reaching55m (QueenslandHerbarium 2015 Tracey 1982)Deciduoustreespeciesarerarehoweverwoodylianasepiphytesand ferns are common resulting in a complex forest structure(Tracey1982)

Volcanicsoilsnamelykrasnozemsoccuronthe level toundu-latingplainsandriseinthestudyregionwhilesteepermountainousareasgenerallycomprisenutrient-poorgraniteandrhyolite-derivedsoils(MalcomNagelSinclairampHeiner1999)

22emsp|emspStudy sites and sampling design

Tensiteswereselectedforstudycomprisingfiveforestfragmentsand five sites innearby intact rain forest (Figure1a)Forest frag-mentswereselectedtominimizevariationintotalarea(23ndash58ha)and thus limit patch-area effects on liana abundance (Lauranceetal 2001 Mohandass etal 2014) comprise remnant forestof similar successionary status (selected using vegetation data

provided by the Wet Tropics Management Authority (WTMA)CairnsAustralia(WTMA2009)themanagingbodyfortheworldheritagearea)andtoensurethattheywereallofasimilarage(cre-ated prior to 1950) and surrounding matrix type (surrounded bycattlepastures)tolessenpossibleconfoundingeffectsoffragmentage or surroundingmatrix type Intact-forest siteswere selectedtobeasspatiallycloseaspossibletothefragmentswiththelarg-estbetween-sitedistanceforallsitesbeinglt23kmandthesmall-estfragmentto intactsitedistance32kmIntersitedistancewasminimizedtolessenvariationinenvironmentalvariablesknowntoinfluencelianaabundanceinparticularrainfallelevationandsoiltype (DeWalt etal 2010 2015 Laurance etal 2001 Schnitzer2005SchnitzerampBongers2002)Theintactforestsiteswerealsointact remnant forestof similar successionary status to the frag-ments (again selected using theWTMA vegetation data) Finallybothfragmentsandintactforestsiteswereselectedtoensuretheywereoverlyingvolcanicsoils(krasnozems)tolimitconfoundingef-fectsofdifferingsoiltypes

Ateachsiteweusedalineartransecttoestablishfive20times20mplotsstratifiedat fivedistanceclassesperpendicular to the forestedge(0ndash2020ndash4040ndash6060ndash80and80ndash100mFigure1b)foratotal(n)of50plotsAteach20mdistanceintotheforestplotswererandomlylocatedalonga100-m-longtransversetransect(Figure1b)toincreasetheirstatisticalindependenceThesmallestdistancebe-tweenplots at any sitewas20m and all plotswere greater than100mfromanyotherforestedgetoavoidconfoundinginfluencesofmultipleforestedges

23emsp|emspLiana measures

FromMarch 2012 to February 2014 liana abundance DBH andclimbingguildweredetermined foreach lianawithinall individualplotsateachof the10sitesLianaabundancewasdeterminedbycountingalllianastemsge1cmDBHwithineachplotUnlessclearlyjoinedstemswereassumedtobeindividuallianaswithnoexcava-tionconductedtodeterminebelowgroundconnectionsTheloca-tion forDBHmeasurementofeach lianastemwasdeterminedbylianagrowthmorphologyaspercurrentmethodology(Gerwingetal2006SchnitzerDeWaltampChave2006SchnitzerRutishauserampAguilar2008)andplot-levelcomparisonsweremadeusingmedianlianasizeperplotAdditionallyeachlianawasassignedtooneoffiveclimbingguildsmainstemtwinerbranchtwinertendrilclimberrootclimberandscrambler(Putz1984b)andtrees(ge10cmDBH)usedasclimbingsupportswereidentifiedandgivenauniquetagnumber

24emsp|emspEnvironmental and structural parameters of fragmented and intact forests

Tocharacterizetheenvironmentalandecologicalconditionsoffrag-mentedandintactforestsitesweexaminedphysicalandstructuralparametersofforestswhichareknowntoinfluencelianaabundanceasidentifiedusingthelianaliteratureanddiscussedinthefollowingparagraphs

TABLE 1emspThemostparsimoniousgeneralizedlinearmixedmodel(binomial)fortheinfluenceofforestfragmentationeffectsandenvironmentalandforeststructuralparametersonproportionaltreeinfestationbylianas

Estimate SE Z value p

Intercept minus1086 0122 minus8881 lt001

Forestedgedistance minus0040 0107 minus0379 704

Quadratictermforestedgedistance(x1 + x2

1)

0234 0102 2286 022

Lianaabundance 0517 0079 6481 lt001

Treeabundance minus0232 0083 minus2798 005

LianaDBH(medianperplot)

0202 0064 3114 001

Canopycover 0216 0091 2364 018

Meanannualrainfall 0161 0063 2528 011

Forestedgedistance=middistanceofplottotheforestedge(m)andthiswasanalyzedusingaquadratictermbasedoninitialresidualdiagnosticsAll explanatory variables were standardized prior to the analysis((xminusmean(x))SD(x))


Toassessforestdisturbancetwomeasureswereexaminedforeachplotcanopycoverandthenumberoffallentrees(ge10cmdi-ameter)Canopy coverwasestimatedat the four corners and thecenterofeachplotandwasmeasuredbyaveragingfoursphericaldensiometer readings taken facing thecardinaldirections (NESW)ateachpoint

Todeterminephysical traits of plotswe examined their slopeandelevationThedegreeofslopeofeachplotwascalculatedusingaclinometerwhileelevationofallsiteswasassessedusingclimaticmodel interpolations data provided by WTMA (WTMA 2009)Thesedatawerealsoassessedtodeterminetheannualrainfall(mm)anddryquarterrainfall(JulyndashSeptembermm)ofsites

Thestructuralparametersoffragmentedandintactforestsiteswereexaminedthroughassessmentoftheresidentrattan(Calamus spp)populationtreepopulationandplot livecarbonstorageas-sessmentRelativerattanabundancewasrecordedforeachplotbyaveragingthecountsofindependentrattanstemsalongfour3-mlonglineintercepttransectslocatedineachcorneroftheexaminedplots(fordetailedmethodsseeCampbelletal2017)

Thetreepopulationwasassessedbycountingalltrees(ge10cmDBH)withineachplotandmeasuringtheirDBHat13mheightoraboveanybuttressesTreeswerealsoscoredintobarktypecatego-riesof ldquosmoothrdquo ldquoroughrdquoor ldquosheddingrdquoandbuttresscategoriesofldquopresentrdquoorldquoabsentrdquoTheseclassificationswerevisuallydeterminedbythesameresearcherthroughoutthestudy(MJC)

Relative live plot carbon storage was estimated by combiningcarbonabovegroundestimatesof all live treesge10cmand lianasge1cmwithinaplot Lianabiomasswascalculatedusing the liana-specific allometric equation (Equation1) developed by Schnitzeretal(2006)

InthismodelD isthediameterat130cmfromtheroots(withthelocationdeterminedasperGerwingetal (2006))expressedincentimeters while AGB is the predicted above ground oven-dryweightofthelianainkilograms

Treeabovegroundbiomass(ABG)wascalculatedusingtheallo-metricequation(Equation2)developedbyChaveetal (2005)(seebelow)asPreeceCrowleyLawesandvanOosterzee(2012)com-paredtheaccuracyofmultiplebiomassestimationmethodsforfor-estswithintheWetTropicsbioregion(withinwhichthestudyareaisfound)andconcludedthattheChaveetal(2005)allometricpro-videdthebestandmostreliableestimatefortheregionToconvertAGB intobiomasscarbonstorageweusedaconversion factorof047whichistherecommendedvaluefromtheIntergovernmentalPanel forClimateChange for tropical forests (IPCC2006) In ad-dition relative AGB was calculated using a single wood densityestimate at the reported default value for Australian tropical for-estsof05gcm3 (500kgm3) (DepartmentofClimateChangeandEnergyDepartmentofClimateChangeandEnergyEfficiency2010)ConsequentlyrelativetreeAGBestimateswerecalculatedusingthefollowingequation

whereAGBismeasuredinkgdbhismeasuredincmandρiswooddensitymeasuredingcm3

Relative above ground biomass estimates for both lianas andtreeswerethenconvertedtorelativecarbonestimates(Equation3)usingtheformula

25emsp|emspData analysis


Disturbanceandforestgapdynamicsalongwiththeavailabilityandsizeoftrees(lianasupports)areknowntobethemajordriversofthedistributionoflianaswithinforests(LedoampSchnitzer2014SchnitzerampBongers2005SchnitzerampCarson2010Schnitzeretal2000)Toassessthesetraitswithinfragmentedandintactforestscanopycover tree abundance and tree DBH were compared along withtheir relationshipswith the previously identified (see above) envi-ronmentalandstructuralparameters(otherthantreebarktypeandbuttressingwhichduetosamplesize limitationswereassessed inlog-linearmodelsbelow)Therelationshipbetweentheseresponsevariablesandtheenvironmentalandstructuralparameterswascom-paredusing individualgeneralized linearmixedmodels (GLMMs) intheglmmADMB (Fournier etal 2012) and lme4 (BatesMaechlerBolkerampWalker2015)packagesGLMMswereselectedtoanalyzethedatagiventhatmultipleexplanatoryfactorssimultaneouslyinflu-encedtheresponsevariablestheresponsevariableswerenonnor-mallydistributedandthesampleunits(plots)werenested(bysite)

PriortomodelgenerationwecheckedforcorrelatedpredictorvariablesfollowingtheprotocolofZuurIenoandElphick(2010)OnevariablewassubsequentlyremovedthemeandryquarterrainfallTopreventundueinfluenceofanyexplanatoryvariableduetounitofmeasurementallexplanatoryvariablesusedinthemodelwerestan-dardized ((xminusmean(x))SD(x)) Standardizing in thismannerhas theadditionalbenefitthattheeffectssizesofallvariablesincludedinthemodelcanbedirectlycomparedviamodelcoefficientsAdditionallyas therewere fiveplotswithin each site (stratifiedby forest edgedistance)plotswerenotfullyindependentAssuchweincludedsiteIDasarandomeffectConsequentlyineachmodel-fittingexerciseweselectedaprioriaglobalmodel inwhichtheresponsevariable(treeabundance treeDBH andcanopycover)wasexaminedas afunction of the following variables (with the response variable re-movedfromthislistintheirrespectiveGLMM)thenumberoffallenlogs(ge10cmdiameter)plotelevation(m)plotslope(degrees)meanannualrainfall(mm)plotdistancetoforestedge(m)meantreeabun-dancetreeDBH(cm)andplotcarbonstorage(tonnesha)relativerattan abundance liana abundance liana DBH and proportionate

(1)AGB=exp [minus1484+2657 ln (D)]

(2)AGB =ρlowast exp (minus1499+2148 ln (dbh)+0207 ( ln (dbh))2

minus00281 ( ln (dbh))3)

(3)Carbon=AGBlowast047


liana infestation of trees canopy cover () tree abundance treeDBH(cm)andtheinteractionbetweentheforesttypeandedgedis-tanceThemostparsimoniousmodelswerethendeterminedusingbackwardsstepwiseregressionwithselectionbasedonlowestAICmodelvaluesusingthedrop1functionofProgramR(RCoreTeam2015)Themostparsimoniousmodelwasdefinedasthatwhichin-cludedtheminimumnumberoftermstoproducethebestpossibleexplanationoftheresponsevariable(lowestAICvalue)andmayormaynot have contained traditionally significant (plt05) variablesTreeabundancewasexaminedusingapoissonGLMMandtreeDBHandcanopycoverwereexaminedusing individual gammaGLMMswithloglinkCanopycoverwasalsologit-transformedpriortomodelinitiation

252emsp|emspThe influence of fragmentation on liana infestation of trees liana abundance and liana DBH

Oncewehadquantifiedthevariationincanopycovertreeabun-danceandtreeDBHbetweenfragmentedandintactforestsandtheirinteractionswiththeenvironmentalandstructuralparame-terswethenconstructindividualGLMMstoidentifytheinfluenceoffragmentationon(i) theproportionoftrees infestedby lianasperplot(ii)lianaabundanceperplotand(iii)lianasize(DBH)Allmodel construction and fittingwas performed as per the previ-ousmethods(seeabove)Theproportionoftreesinfestedbylia-naswasexaminedusingabinomialGLMMwitha logit link lianaabundanceusinganegativebinomialGLMMand the lianaDBHexaminedusingagammaGLMMwithloglinkFurthermorewhereexaminationoftheresidualsfromthefinalmodelrevealedincor-rectmodelfitmodelfitwasfurtherimprovedbyincludingaquad-ratic term This occurred after checking residual diagnostics formodelsdescribingtheproportionof trees infestedby lianasandlianaabundancewithcurvatureinbothcasesrelatedtodistancetotheforestedge(seeSection3)

253emsp|emspHost- tree morphology and forest effects

Alog-linearmodel(Poissonwithloglink)wasusedtodeterminetherelationshipbetweenhost-treemorphologicaltraitsandtheimpactofforesteffectsThesewereassessedbyexaminingtherelationshipbetweenthecategoricalvariablesoftreebuttresspresence(yesorno)treebarktype(smoothroughorshedding)foresttype(frag-mentedorintact)distancetotheforestedge(0ndash2020ndash4040ndash6060ndash80and80ndash100m)andwhetheratreewasinfestedbyoneormorelianas(yesorno)

254emsp|emspInfesting liana climbing guilds forest type and environmental traits

Todeterminetherelationshipbetweeninfestinglianatraitsandtheimpactof foresteffectsweuseda log-linearmodelas in the tree-hosttraitsmodelaboveWecomparedthecategoricalvariableslianaclimbingguildtype (branchclimberhookclimbermainstemtwiner

rootclimberscramblertendrilclimberunknown)foresttype(frag-mentedorintact)distancetotheforestedge(0ndash2020ndash4040ndash6060ndash80and80ndash100m)andwhetheratreewasinfestedbylianas(yesorno)AllanalyseswereperformedinProgramR(RCoreTeam2015)

3emsp |emspRESULTS


Treeabundancewassignificantlylowerinfragmentedforeststhaninintactforestsbutwashigheronforestedgesthanonforestinte-riors (seeTableS1)Asexpectedtreeabundancewassignificantlyandpositivelyrelatedtorelativeforestcarbonhoweveritwassig-nificantlyandnegativelyrelatedtoaltitude(TableS1)

Tree size (DBH)was significantly higher in fragmented foreststhaninintactforestsandwasalsohigherinsiteswithgreatercanopycoverathigheraltitudewherelargelianaswerepresentandsiteswithgreaterrelativeforestcarbon(seeTableS2)

Canopycoverwassignificantly lower in fragmented that in in-tactforestsandwasloweronforestedgesthanonforestinteriors(seeTableS3)Thereduction incanopycoveralsopenetratedsig-nificantly further intotheedgesof fragmentedthan intact forests(TableS3)Canopycoverwasalsofoundtobesignificantlyandneg-ativelyrelatedtoaltitude(TableS3)

32emsp|emspEnvironmental and structural predictors of tree infestation by lianas

Treeinfestationbylianaswasnotsignificantlyrelatedtoforesttype(fragmentedorintact)(Table1)withanaverageof~29(SEplusmn0024)oftreesinfestedinfragmentsand~32(SEplusmn0029)inintactforestTreeinfestationbylianaswassignificantlyandpositivelyrelatedtoin-creasinglianaabundancelianaDBHcanopycoverandmeanannualrainfall(Table1Figure2)Oftheseparameterslianaabundancehadthegreatest influenceontheproportional liana infestationof treeswiththehighestrelativeeffectsizeof0517(SEplusmn0079)(Table1)Treeinfestationbylianassignificantlydecreasedwithincreasingtreeabun-dancebutwasparabolicallyrelatedtotheforestedgedistancewithmore trees infestedby lianason forestedgesand in forest-interiorplotsandfewerinthoseplotsinbetween(Table1Figure2)

33emsp|emspEnvironmental and structural predictors of liana abundance

Atthelandscapelevelwerecordedatotallianaabundanceof2124(n)stemsLianaabundancewassignificantlyandpositivelyrelatedtoforestfragmentationandanincreaseinthenumberoffallenlogsinaforest(Table2Figure3)Howeverlianaabundancesignificantlyde-creasedwithanincreaseinforestcarbonstorage(Table2Figure3)Lianaabundancewasalsosignificantlyandparabolicallyrelatedtoforestedgedistancewithmorelianasonforestedgesandinforest-interiorplotsandfewerinthoseplotsinbetween(Table2Figure3)


Moreover therewasasignificant interactionbetweenforest type(fragmentedor intact)andthedistancetothenearestforestedge(Table2 Figure3) Of all parameters tested forest-edge distancehadthelargest influenceonlianaabundancewitharelativeeffectsizeofminus0750(SEplusmn0162)(Table2)

34emsp|emspEnvironmental and structural predictors of liana DBH

Liana DBH was significantly and positively related to both tree-infestationratesandtreeDBHandtherewasapositivebutnon-significant relationship between liana DBH and tree abundance(Table3Figure4)ConverselylianaDBHwasnegativelyrelatedtoanincreaseinlianaabundanceandsiteslope(Table3Figure4)Oftheexaminedparametersthenumberofliana-infestedtreeshadthelargest positive influence on lianaDBHwith a relative effect sizeof0137(SEplusmn0034Table3)Converselylianaabundancewasthemostnegativelyrelatedparameterto lianaDBHwitharelativeef-fectsizeofminus0115(SEplusmn0037)(Table3)

35emsp|emspHost- tree morphology and forest effects on liana- infestation rates

Theprobabilityofatreehostingalianawasprimarilydeterminedbyitsdistancetotheforestedgewithfragmentationstatustreebarktypeorpossessionofbuttresseshavingalimitedaffect(Table4)

F I G U R E 2emspTherelationshipbetweenproportionaltreeinfestationbylianasand(a)lianaabundance(b)lianaDBH(medianperplot)(c)treeabundance(d)canopycover(e)meanannualrainfalland(f)midplotdistancetotheforestedgeThetrendlinesarepredictedvaluesandshadedareasrepresentthe95confidenceintervals

TABLE 2emspThemostparsimoniousgeneralizedlinearmixedmodel(negativebinomial)fortheinfluenceofforestfragmentationeffectsandenvironmentalcharacteristicsonlianaabundance


Intercept 2839 0186 1525 lt001

Forestedgedistance(m)

minus0750 0162 minus461 lt001


1)

0499 0116 427 lt001

Foresttype(Fragmented)

0427 0202 211 035

Treeabundance 0180 0122 147 140

Carbon minus0307 0083 minus368 lt001

Altitude 0156 0092 170 089

Fallenlogs 0156 0078 201 044

Canopycover 0246 0142 173 083

Forestedgedistanceforesttypeinteraction

0520 0164 316 001




Lianasthat infestedtreesvariedbyboththeirdistancetothefor-est edge and fragmentation status of the forest patch (Table5)Moreover there was a significant variation in the abundance oflianaswithinindividualclimbingguildsanddifferencesbetweenre-sponsesofdifferentclimbingguildswereassociatedwithboththedistancetotheforestedgeandforestfragmentation(Table5)

4emsp |emspDISCUSSION

41emsp|emspLiana abundance and habitat fragmentation

Fromourresultsitisclearthatforestedgedisturbanceandhabitatfragmentationhavesignificantlyalteredthelianacommunityandtheecologicalrelationshipbetweenlianasandtreeswithinrainforestsof

theAthertonTablelandWefoundforestfragmentationresultedinasignificant increase in lianaabundanceFurthermorewhereas lianaabundancewassignificantlyhigherontheedgesofbothforesttypesthiseffectpenetratedfurtherintotheedgesoffragmentedthanin-tactforestsItislikelythattheincreaseinlianaabundanceatgreaterdistances within fragmented forests is primarily due to increaseddisturbanceonfragmentedgesForexamplecanopycoverwassig-nificantlylesswithinfragmentedforeststhaninintactforests(TableS3)Furthermorecanopycoverdecreasedsignificantlyinresponsetoproximitytotheforestedgeinbothforesttypesbutthisoccurredatasignificantlygreaterrateinfragmentedforests(TableS3)Adecreaseincanopycoverwhichisfoundonforestedgesorintreefallgapsiswellknowntofavorlianaproliferationoftenattheexpenseoftreerecruitmenttreesuccessiontreegrowthandforestcarbonstorage(SchnitzerampCarson20012010Schnitzeretal20002014)

Lianaabundancealsosignificantlyincreasedwithincreasingfre-quencyoffallenlogs(ge10cmdiameter)withinaplotanindicatorof

F I G U R E 3emspTherelationshipbetweenlianaabundanceandtheinteractionofforesttypeand(a)distancetothenearestforestedge(b)fallenlogsand(c)storedforestcarbon(log10-transformed)TheindividualtrendlinesarepredictedvaluesandshowthesignificantinteractionforesttypeandforestedgedistanceShadedareasrepresentthe95confidenceintervals

Estimate SE t value p

Intercept 0542 0026 2056 lt001

Proportionatelianainfestationoftrees 0137 0034 397 lt001

Lianaabundance minus0115 0037 minus311 001

Treediameterbreastheight(DBH) 0073 0028 255 010


Slope minus0081 0027 minus294 003

Lianadiameterbreastheight(cm)wasmeasuredaspercurrentstandardprotocols(Gerwingetal2006Schnitzeretal20062008)Allexplanatoryvariableswerestandardizedpriortotheanalysis((xminusmean(x))SD(x))

TABLE 3emspThemostparsimoniousgeneralizedlinearmixedmodel(gammaloglink)fortheinfluenceofforestfragmentationeffectsandenvironmentalcharacteristicsonlianadiameterbreastheight(medianperplot)


past forestdisturbance (egAttiwill1994)Moreover lianaabun-dancesignificantlydecreasedwithincreasingforestcarbonstoragewhich is strongly positively associatedwith the presence of largetrees(Sliketal2013)indicativeoflowratesofforestdisturbance(LauranceFerreiraRankin-deMeronaampLaurance1998Lauranceetal200020022006a)Numerousstudieshaveshownthatfrag-ment edgesexperiencehigher levelsof disturbance than thoseofintactforests(egHarperetal2005Lauranceetal20112018Saundersetal1991TabarelliLopesampPeres2008)withothersidentifying localized forest disturbance as the primary driver oflocallianaabundancewithinaforest(Lauranceetal2001Ledoamp

Schnitzer2014Schnitzer2015SchnitzerampBongers2011)Thusourresultsoflianaabundanceincreasinginfragmentsinresponsetodisturbancearesupportedbypreviousfindingsoflianaproliferationduetoincreaseinforestdisturbance(LedoampSchnitzer2014)

42emsp|emspLiana infestation of trees

Theproportionoftreesinfestedbylianasdidnotdiffersignificantlybetween fragmentedand intact forestsNevertheless lianaabun-dancewasa significantpredictorof the infestation ratesof treesAsdistancetotheforestedgestronglyinfluenceslianaabundance

F I G U R E 4emspTherelationshipbetweenlianadiameterbreastheight(DBHmedianperplot)and(a)proportionoftreesinfestedbylianas(b)lianaabundance(c)treeDBH(d)treeabundanceand(e)slopeThetrendlinesarepredictedvaluesandshadedareasrepresentthe95confidenceintervals

TABLE 4emspTheanalysisofdevianceforalog-linearmodelinvestigatingassociationbetweentreesinfestedwithlianas(yesorno)foresttype(fragmentedorintact)distancetotheforestedge(0ndash2020ndash4040ndash6060ndash80and80ndash100m)buttresspresence(yesorno)andbarktype(smoothroughorshedding)

df Deviance Residual df Residual deviance p

Null NA NA 119 3005451 NA

Treeinfested 1 220284 118 2785166 lt001

Foresttype 1 17823 117 2767343 lt001

Edge 4 32012 113 2735331 lt001

Barktype 2 2549900 110 184913 lt001

Treeinfestededge 4 32352 105 149761 lt001

Forestbuttress 1 6529 99 140136 011

Buttressbark 2 11811 81 111681 003

Forestedgebuttress 4 9627 68 84437 047

Treeinfestedforestbuttressbark 2 6704 28 20991 035

dfdegreesoffreedomOnlysignificantfindingsaredisplayed


increaseddisturbanceneartheedgesofforestfragmentsisnotonlydrivingdifferencesinthespatialpatternoflianaconcentrationsbutalsotheprobabilitythatindividualtreeswillbeinfested(Laurance1997aLauranceetal2001)Infactstudiessuggestthatthemereproximityoflianastopotentialhosttreesmaybeaprimarydetermi-nantofhosttreeselectionbylianas(Roederetal2015)andthusanincreaseinlocallianaabundance(duetoforestdisturbance)wouldleadtoanincreaseinlocaltreeinfestationprobabilities

Theprobabilityoftreesinfestationbylianaswasalsosignificantlyinfluencedbythesizeoflianas(DBH)withahigherfractionoftreesinfestedatsiteswithalargermedianlianasizethanatsiteswithasmallermedianlianasizeThecorrelationbetweenlianasizeandtreeimpactwaspreviouslynotedbyPutzwhoobservedthatthereisastrongcorrelationbetweenlianadiameterandlianaleafarea(Putz1983)andthustheeffectsoflianasontheirsupportingtrees(Putz1984b)Howeverunlike lianaabundancemedian lianasizewithinafragmentwaspositivelyrelatedtodecreaseddisturbanceandtheprevalenceofmatureforesttraits(HegartyampCaballe1991Letcher2015)Wefoundmedian lianasize (DBH)tobepositivelyandsig-nificantlyrelatedtofactorsassociatedwithmaturesuccessionalfor-esttraitssuchaslargertreediameterincreasingcanopycoveranddecreasingtreeabundanceThereforewhilesiteswithlargerlianas(DBH)significantlycontributedtotreeinfestationratestheirprev-alencewassignificantlyrelatedtoareasofforestwithmatureforesttraits(HegartyampCaballe1991Letcher2015)

Asbothincreasedlianaabundanceandsize(DBH)significantlycontributed to liana infestation ratesof treeswithin a forest it islikely that patterns of disturbance and subsequent forest succes-sion combine to determine liana infestation rates of trees withinforest fragmentsForexample initial forestdisturbancecanfacili-tatelianarecruitmentandabundance(LedoampSchnitzer2014)withsubsequentforestcanopyclosureintheseareasresultingin lianas

intheforestcanopy(ieingeneralthosege2cmKurzelSchnitzerampCarson2006)beingretainedandincreasinginsizebutthecan-opyclosureprecludingadditional lianastemssuccessfullyreachingthecanopy(Letcher2015LetcherampChazdon2009Putz1984b)Consequentlytreeinfestationandlianasizedistributionswithinfor-estfragmentslikelyreflectforestdynamicsandlianacommunityagewithdistinctdifferencesincommunitycompositionbetweenlargerlianas in older (less disturbed) areas and smaller lianas in youngerforestsections(ierecentlydisturbed)(Letcher2015)

43emsp|emspInfesting liana climbing guilds and host tree traits and their response to forest effects

Lianainfestationoftreeshaspreviouslybeenlinkedtothemorpholog-icalandecologicaltraitsoflianasthemselves(egthepreferredsizeofclimbingtrellisesusedbydifferentliana-climbingguildsPutz1984bPutzampChai1987)Wefoundfragmentationoftherainforestsignifi-cantlyinfluencedlianainfestationoftreesandtheseeffectsinturnresultedinsubstantialshiftsintherelativeabundanceoflianaclimb-ingguildsProportionsoftotalstemsindifferentlianaclimbingguildsvariedsignificantlyinresponsetoforestedgedistancewithinandbe-tweenbothfragmentedandintactforests It is likelythatthevaria-tioninlianaguildcompositionbetweenfragmentedandintactforestscanagainbeattributedto increaseddisturbanceoffragmentedfor-estedges(Laurance1997aLauranceampCurran2008Oliveiraetal1997Tabarellietal2008)Disturbanceisknowntoresultinthepro-liferationofusuallysmallersuccessionaltreesandearliersuccessionalforests(Chazdon2014Laurance1997a2002Lauranceetal20022006bTabarellietal2008)Theserecruitsincreasetheavailabilityofsmaller-sizedclimbingtrellises(iesmalltreesandbranches)whicharefavoredbytendrilclimbersandstemtwinerswhichalsoproliferatethereLianasthatutilizelargerclimbingtrellises(egbranchtwiners)



Forest 1 12064 138 3031484 lt001

Guild 6 1032740 132 1998744 lt001

Edge 4 679871 128 1318874 lt001

Infestingliana 1 75781 127 1243092 lt001

Forestguild 6 95485 121 1147607 lt001

Forestedge 4 97822 117 1049785 lt001

Guildedge 24 341774 93 708012 lt001

Forestinfestingliana 1 7825 92 700187 005

Guildinfestingliana 6 211509 86 488678 lt001

Edgeinfestingliana 4 14513 82 474165 006

Forestguildedge 24 372679 58 101486 lt001

Forestguildinfestingliana

6 22505 52 78981 lt001

Guildedgeinfestingliana

24 42878 28 36103 010

dfdegreesoffreedomNonsignificanthigher-interactiontermswereremoved

TABLE 5emspTheanalysisofdevianceforalog-linearmodelinvestigatingassociationbetweenforesttype(fragmentedorintact)lianaclimbingguild(branchclimberhookclimbermainstemtwinerrootclimberscramblertendrilclimberunknown)distancetotheforestedge(0ndash2020ndash4040ndash6060ndash80and80ndash100m)whetherthelianainfestedatree(yesorno)


aremorefrequentlyfoundinmatureforest(Putz1984bPutzampChai1987SchnitzerampBongers2002)Consequentlymuchofthechangesin lianacommunitycompositionand infestationrates infragmentedforestscanbeattributedtotheeffectsofdisturbanceindeterminingtheavailabilityofdifferent-sizedclimbingtrellises

Morphological attributesof treeshavealsobeensuggested toinfluencetheprobabilityoflianainfestationForbothtreebarktype(BoomampMori1982Putz1980) andbuttresspresence (BoomampMori1982Putz1980)havebeennotedaspotentiallianainhibitorsForinstanceithasbeensuggestedthatflakybarkedtreesmayshedlianaswhile smoothbark treesmaydecrease the successof lianaattachment(Putz1984b)Meanwhiletreebuttressinghasbeenhy-pothesizedtoactasamechanicalbarrierpreventinglianaproximityandthereforeattachment(BlackampHarper1979)Howeverashasbeenfoundinpreviousstudies(BoomampMori1982Putz1980)wefoundthatneithertreebarktypenorbuttresspresencesignificantlyinfluencedtheprobabilityofhostingaliana

44emsp|emspPrediction of future liana impacts upon fragmented forests

It is clear thatmultiple environmental and ecological determinantsinfluence liana infestationoftrees (Hegarty1991vanderHeijdenetal2008Putz19801984a1984bSchnitzerampBongers2002)and that these determinants likely interact synergistically (van derHeijdenetal2008Lauranceetal2014aSfairetal2016)Furtherattributesofthelianacommunity(abundancesizedistributionclassand climbing guild) all respond to these influences Neverthelesslianaabundancealoneisoftenusedasaproxytoinferlikelylianaim-pact(andfutureimpact)onfragmentedforests(egCampbelletal2015a 2015b Schnitzer Bongers ampWright 2011Wright 2010)HoweverourfindingsidentifiedlianasizeasapossibleindicatorofpotentiallianainfestationratesoftreesandfuturelianaimpactLianasareknowntosignificantlyimpactforestcommunityprocessessuchasdecreasingforestcarbonstoragecapacity(Schnitzeretal2014vanderHeijdenetal 2013vanderHeijdenPhillipsampSchnitzer2015avanderHeijdenPowersampSchnitzer2015b)arrestingforestsuccession(PaulampYavitt2011SchnitzerampBongers2005SchnitzerampCarson2010Tymenetal2015)andcausingdifferentialmortal-itybetweenhostspecies(ClarkampClark1990SchnitzerampBongers2002) However the contribution to these impactsmade by largelianasisoftennotdeterminedAndasabovemostfocusisonlianaabundance Consequently when assessing tropical closed-canopyforestsforlianaimpactsanddeterminingfuturemanagementstrate-giesaswellastheclearlyjustifiableassessmentofoveralllianaabun-danceconsiderableusefulinformationmaybeattainedthroughtheassessmentofthelianasize(DBH)frequencydistributionsatsites

5emsp |emspCONCLUSION

Forestfragmentationsignificantlyalterstheabundanceandcom-munity composition of lianas and their ecological relationships

with trees Liana abundance increased significantlywithin frag-mentedforestsinresponsetotheincreaseddisturbanceoffrag-mented forest edges However liana infestation rates of treeswere not significantly different between fragmented and intactforestsbutwasinfluencedbylianaabundanceandaveragelianasize (DBH) Abundance and size distribution responded in op-posingways toenvironmentaldriverspotentiallyexplaining thefinding of no significant difference in infestation rates of treesexistinginfragmentedandintactforestsMoreovertheincreaseddisturbanceofforestedgesresultedinashiftinthecompositionoflianaclimbingguildslikelyduetoachangeinthesizeofavail-ableclimbingtrellisesFinallyourfindingsclearlyidentifythefactthateffectivecontroloflianasinforestfragmentsrequiresman-agementpracticeswhichdirectlyfocusonminimizingforestedgedisturbance

ACKNOWLEDG MENTS

MJCreceivedfundingfromaCowanBursaryAMwasfundedbyaBasqueGovernment postdoctoral fellowshipWFLwas supportedby an Australian Laureate Fellowship and an Australian ResearchCouncilDiscoverygrant

CONFLIC T OF INTERE S T

Nonedeclared

AUTHOR CONTRIBUTION

MJCWEandWFLconceivedtheideaanddesignedthepro-jectMJCandAMcollectedthedataMJCWEAMandGPanalyzedthedataMJCdraftedthearticleandallauthors(includ-ingDM)contributedtocriticalrevisionsofthemanuscript

ORCID

Mason J Campbell httporcidorg0000-0001-6803-271X

R E FE R E N C E S

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Arroyo-RodriguezVampToledo-AcevesT (2009) Impactof landscapespatial pattern on liana communities in tropical rainforests at LosTuxtlasMexicoApplied Vegetation Science12340ndash349httpsdoiorg101111j1654-109X200901030x


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CampbellMLauranceWFampMagrachA(2015a)Ecologicaleffectsof lianas in fragmented forests In S A Schnitzer F Bongers RBurnhamampFEPutz(Eds)Ecology of lianas(pp447ndash454)OxfordWiley-BlackwellPublishing

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DeWaltSJSchnitzerSAChaveJBongersFBurnhamRJCaiZQhellipThomasD (2010)Annual rainfallandseasonalitypredictpan-tropicalpatternsoflianadensityandbasalareaBiotropica42309ndash317httpsdoiorg101111j1744-7429200900589x

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Garrido-PerezEIampBurnhamRJ(2010)Theevolutionofhostspeci-ficityinliana-treeinteractionsPuente Biologico3145ndash157

Gerwing J J Schnitzer S A Burnham R J Bongers F ChaveJ DeWalt S J hellip Thomas D W (2006) A standard proto-col for liana censuses Biotropica 38 256ndash261 httpsdoiorg101111j1744-7429200600134x

Gibson L Lynam A J Bradshaw C J A He F Bickford D PWoodruffDShellipLauranceWF(2013)Near-completeextinctionofnativesmallmammalfauna25yearsafter forest fragmentationScience3411508ndash1510httpsdoiorg101126science1240495

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HarperKAMacdonaldSEBurtonPJChenJBrosofskeKDSaundersSChellipEsseenP-A(2005)Edgeinfluenceonforeststruc-tureandcompositioninfragmentedlandscapesConservation Biology19768ndash782httpsdoiorg101111j1523-1739200500045x

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van der Heijden G M F Phillips O L amp Schnitzer S A (2015a)Impactsof lianasonforest-levelcarbonstorageandsequestrationInSASchnitzerFBongersRBurnhamandFEPutz(Eds)Ecology of lianas(pp164ndash174)OxfordJohnWileyampSonsLtd

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IngwellLLWrightSJBecklundKKHubbellSPampSchnitzerSA (2010) The impact of lianas on10 years of tree growth andmortalityonBarroColoradoIslandPanamaJournal of Ecology98879ndash887httpsdoiorg101111j1365-2745201001676x

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LauranceW F (1997a) Hyper-disturbed parks Edge effects and theecology of isolated rainforest reserves in tropical Australia InWF LauranceampROBierregaard Jr (Eds)Tropical forest remnants Ecology management and conservation of fragmented communities(pp71ndash83)ChicagoTheUniversityofChicagoPress

LauranceWF(1997b)Responsesofmammalstorainforestfragmenta-tionintropicalQueenslandAreviewandsynthesisWildlife Research24603ndash612httpsdoiorg101071WR96039

Laurance W F (2002) Hyperdynamism in fragmented habi-tats Journal of Vegetation Science 13 595ndash602 httpsdoiorg101111j1654-11032002tb02086x

LauranceWFAndradeASMagrachACamargoJLCCampbellMFearnsidePMhellipLauranceSG (2014a)Apparentenviron-mental synergism drives the dynamics of Amazonian forest frag-mentsEcology953018ndash3026httpsdoiorg10189014-03301

LauranceWFAndradeASMagrachACamargoJLCValskoJ J CampbellM hellip Laurance S G (2014b) Long-term changesin lianaabundanceand forestdynamics inundisturbedAmazonianforestsEcology951604ndash1611httpsdoiorg10189013-15711

Laurance W F Camargo J L C Fearnside P M Lovejoy T EWilliamsonGBMesquitaRCGhellipLauranceSGW (2018)AnAmazonianrainforestanditsfragmentsasalaboratoryofglobalchange Biological Reviews 93 223ndash247 httpsdoiorg101111brv12343

LauranceWFCamargoJLCLuizatildeoRCCLauranceSGPimmSLBrunaEMhellipLovejoyTE(2011)ThefateofAmazonianfor-estfragmentsA32-yearinvestigationBiological Conservation14456ndash67httpsdoiorg101016jbiocon201009021

LauranceWFampCurranTJ(2008)ImpactsofwinddisturbanceonfragmentedtropicalforestsAreviewandsynthesisAustral Ecology33399ndash408httpsdoiorg101111j1442-9993200801895x

LauranceWFDelamonicaP LauranceSGVasconcelosHLampLovejoy T E (2000) Conservation Rainforest fragmentation killsbigtreesNature404836httpsdoiorg10103835009032

LauranceWFFerreiraLVRankin-deMeronaJMampLauranceSG(1998)RainforestfragmentationandthedynamicsofAmazoniantreecommunitiesEcology792032ndash2040httpsdoiorg1018900012-9658(1998)079[2032RFFATD]20CO2

LauranceWFLauranceSGFerreiraLVRankin-deMeronaJMGasconCampLovejoyTE (1997)Biomasscollapse inAmazonianforestfragmentsScience2781117ndash1118httpsdoiorg101126science27853401117

LauranceWFLovejoyTEVasconcelosHLBrunaEMDidhamRKStoufferPChellipSampaioE(2002)EcosystemdecayofAmazonianforestfragmentsA22-yearinvestigationConservation Biology16605ndash618httpsdoiorg101046j1523-1739200201025x

LauranceWFNascimentoHEMLauranceSGAndradeACFearnside PM Ribeiro J E LhellipFearnside PM (2006b) Rainforest fragmentation and the proliferation of successional treesEcology87469ndash482httpsdoiorg10189005-0064

Laurance W F Nascimento H E M Laurance S G AndradeA Ribeiro J E L SGiraldo J PhellipDrsquoAngelo S (2006a) Rapiddecay of tree-community composition in Amazonian forest frag-mentsProceedings of the National Academy of Sciences of the United States of America 103 19010ndash19014 httpsdoiorg101073pnas0609048103

Laurance W F Perez-Salicrup D Delamonica P Fearnside P MDrsquoAngelo S Jerozolinski A hellip Lovejoy T E (2001) Rain forestfragmentation and the structure of Amazonian liana communitiesEcology82 105ndash116 httpsdoiorg1018900012-9658(2001)082[0105RFFATS]20CO2

Ledo A amp Schnitzer S A (2014) Disturbance and clonal repro-duction determine liana distribution and maintain liana diver-sity in a tropical forest Ecology 95 2169ndash2178 httpsdoiorg10189013-17751

LetcherSG(2015)PatternsoflianasuccessionintropicalforestsInSASchnitzerFBongersRJBurnhamandFEPutz(Eds)Ecology of lianas(pp116ndash130)OxfordJohnWileyampSonsLtd

LetcherSGampChazdonRL(2009)Lianasandself-supportingplantsduring tropical forest succession Forest Ecology and Management2572150ndash2156httpsdoiorg101016jforeco200902028

Londre R A amp Schnitzer S A (2006) The distribution of li-anas and their change in abundance in temperate forestsover the past 45 years Ecology 87 2973ndash2978 httpsdoiorg1018900012-9658(2006)87[2973TDOLAT]20CO2

MagnagoLFSMagrachABarlowJSchaeferCEGRLauranceWFMartinsSVampEdwardsDP(2016)Dofragmentsizeandedgeeffectspredictcarbonstocksintreesandlianasintropicalfor-estsFunctional Ecology31542ndash552

MagnagoLRochaMMeyerLMartinsSampMeira-NetoJ(2015)Microclimaticconditionsatforestedgeshavesignificantimpactsonvegetationstructure in largeAtlantic forest fragmentsBiodiversity and Conservation 24 2305ndash2318 httpsdoiorg101007s10531-015-0961-1

MagrachALauranceWFLarrinagaARampSantamariaL(2014a)Meta-analysis of the effects of forest fragmentation on interspe-cific interactionsConservation Biology28 1342ndash1348 httpsdoiorg101111cobi12304

Magrach A Rodriacuteguez-Peacuterez J Campbell M amp Laurance W F(2014b) Edge effects shape the spatial distribution of lianasand epiphytic ferns in Australian tropical rain forest fragmentsApplied Vegetation Science17 754ndash764httpsdoiorg101111avsc12104

Maier F (1982) Effects of physical defenses on vine and epiphytegrowthinpalmsTropical Ecology23212ndash217

MalcomDTNagelBKASinclairIampHeinerIJ(1999)Soils and ag-ricultural land suitability of the Atherton Tablelands north Queensland BrisbaneDepartmentofNaturalResources

MohandassDCampbellMJHughesACMammidesCampDavidarP(2017)Theeffectofaltitudepatchsizeanddisturbanceonspe-ciesrichnessanddensityof lianas inmontaneforestpatchesActa Oecologica831ndash14httpsdoiorg101016jactao201706004

MohandassDHughesACCampbellMampDavidarP(2014)Effectsofpatchsizeonlianadiversityanddistributionsinthetropicalmon-tane evergreen forests of the Nilgiri Mountains southern IndiaJournal of Tropical Ecology 30 579ndash590 httpsdoiorg101017S0266467414000455

MurciaC (1995)Edgeeffects in fragmented forests Implications forconservationTrends in Ecology amp Evolution10 58ndash62 httpsdoiorg101016S0169-5347(00)88977-6

Muthuramkumar S Ayyappan N Parthasarathy N MudappaD Raman T R S Selwyn M A amp Pragasan L A (2006)Plant community structure in tropical rain forest fragments ofthe Western Ghats India Biotropica 38 143ndash160 httpsdoiorg101111j1744-7429200600118x


OliveiraATdeMelloJMampScolforoJRS(1997)Effectsofpastdisturbanceandedgeson treecommunitystructureanddynamicswithinafragmentoftropicalsemideciduousforestinsouth-easternBraziloverafive-yearperiod(1987-1992)Plant Ecology13145ndash66httpsdoiorg101023A1009744207641

OliveiraMASantosAMMampTabarelliM(2008)Profoundimpov-erishmentofthelarge-treestandinahyper-fragmentedlandscapeoftheAtlanticforestForest Ecology and Management2561910ndash1917httpsdoiorg101016jforeco200807014

OuedraogoISavadogoPTigabuMColeROdenPCampOuadbaJM(2011)Trajectoryanalysisofforestcoverchangeinthetropi-caldryforestofBurkinaFasoWestAfricaLandscape Research36303ndash320httpsdoiorg101080014263972011564861

PasquiniSCWrightSJampSantiagoLS(2015)Lianasalwaysout-perform tree seedlings regardless of soil nutrients Results from along-termfertilizationexperimentEcology961866ndash1876httpsdoiorg10189014-16601

PaulGSampYavitt JB (2011)Tropicalvinegrowthand theeffectson forest successionA reviewof theecologyandmanagementoftropicalclimbingplantsThe Botanical Review7711ndash30httpsdoiorg101007s12229-010-9059-3

Pearson L (2008) The log trade in far north Queensland BrinsmeadQueenslandPearsonLMBrinsmead

PehK SH Lin Y Luke SH FosterWAampTurner EC (2014)ForestfragmentationandecosystemfunctionInCJKettleampLPKoh(Eds)Global forest fragmentation(pp96ndash114)WallingfordCABI

Perez-Salicrup D R amp Barker M G (2000) Effect of liana cut-ting on water potential and growth of adult Senna multijuga(Caesalpinioideae)treesinaBoliviantropicalforestOecologia124469ndash475httpsdoiorg101007PL00008872

Perez-SalicrupDRampdeMeijereW(2005)NumberoflianaspertreeandnumberoftreesclimbedbylianasatLosTuxtlasMexicoBiotropica37153ndash156httpsdoiorg101111j1744-7429200503223x

Peacuterez-SalicrupDRSorkVLampPutzFE(2001)LianasandtreesinalianaforestofAmazonianBoliviaBiotropica3334ndash47httpsdoiorg101111j1744-74292001tb00155x

PowersJSKalicinMHampNewmanME(2004)Treespeciesdonotinfluence local soil chemistry in a species-richCostaRica rain for-estJournal of Tropical Ecology20587ndash590httpsdoiorg101017S0266467404001877

PreeceNDCrowleyGMLawesMJampvanOosterzeeP(2012)Comparing above-ground biomass among forest types in theWetTropics Small stems and plantation types matter in carbon ac-countingForest Ecology and Management264228ndash237httpsdoiorg101016jforeco201110016

PutzFE (1980)LianasVStreesBiotropica12224ndash225httpsdoiorg1023072387978

PutzFE(1983)LianabiomassandleafareaofaldquoTierraFirmerdquoforestintheRioNegroBasinVenezuelaBiotropica15185ndash189httpsdoiorg1023072387827

PutzFE(1984a)HowtreesshedandavoidlianasBiotropica1619ndash23httpsdoiorg1023072387889

PutzFE(1984b)ThenaturalhistoryoflianasonBarro-ColoradoislandPanama Ecology651713ndash1724httpsdoiorg1023071937767

Putz F E (1990) Growth habits and trellis requirements of climbingpalms(Calamusspp)innorth-easternQueenslandAustralian Journal of Botany38603ndash608httpsdoiorg101071BT9900603

Putz F E amp Chai P (1987) Ecological-studies of lianas in LambirNational-Park SarawakMalaysia Journal of Ecology75 523ndash531httpsdoiorg1023072260431

RCoreTeam(2015)R A language and environment for statistical comput-ing (EdRCoreTeam)ViennaAustriaRFoundationforStatisticalComputing

ReidJPSchnitzerSAampPowersJS (2015)Shortand long-termsoilmoistureeffectsof lianaremoval inaseasonallymoisttropical

forest PLoS ONE 10 e0141891 httpsdoiorg101371journalpone0141891

RibeiroMCMetzgerJPMartensenACPonzoniFJampHirotaMM(2009)TheBrazilianAtlanticforestHowmuchisleftandhowis the remaining forest distributed Implications for conservationBiological Conservation 142 1141ndash1153 httpsdoiorg101016jbiocon200902021

RichPMLumSMunozLampQuesadaM(1987)SheddingofvinesbythepalmsWelfia georgiiandIriartea gigantea Principes3131ndash34

Riitters K Wickham J Costanza J K amp Vogt P (2016) A globalevaluation of forest interior area dynamics using tree cover datafrom 2000 to 2012 Landscape Ecology 31 137ndash148 httpsdoiorg101007s10980-015-0270-9

Rodriacuteguez-RonderosMEBohrerGSanchez-AzofeifaAPowersJSampSchnitzerSA(2016)ContributionoflianastoplantareaindexandcanopystructureinaPanamanianforestEcology973271ndash3277httpsdoiorg101002ecy1597

RoederMSlikJWFHarrisonRDPaudelEampTomlinsonKW(2015)Proximity to thehost isan importantcharacteristic for se-lectionofthefirstsupportinlianasJournal of Vegetation Science261054ndash1060httpsdoiorg101111jvs12316

SaundersDAHobbsRJampMargulesCR(1991)Biologicalconse-quencesofecosystemfragmentationAreviewConservation Biology518ndash32httpsdoiorg101111j1523-17391991tb00384x

SchnitzerSA(2005)AmechanisticexplanationforglobalpatternsoflianaabundanceanddistributionAmerican Naturalist166262ndash276httpsdoiorg101086431250

SchnitzerSA(2015)IncreasinglianaabundanceinneotropicalforestsCausesandconsequencesInSASchnitzerFBongersRBurnhamandF E Putz (Eds)Ecology of lianas (pp 451ndash464)Oxford JohnWileyampSonsLtd

Schnitzer S A ampBongers F (2002) The ecology of lianas and theirroleinforestsTrends in Ecology amp Evolution17223ndash230httpsdoiorg101016S0169-5347(02)02491-6

SchnitzerSampBongersF (2005)LianasandgapphaseregenerationImplicationsforforestdynamicsandspeciesdiversityInFBongersM P E Parren amp D Traore (Eds) Forest climbing plants of West Africa Diversity ecology and management (pp 59ndash72)WallingfordCABIPublishinghttpsdoiorg10107997808519991420000

Schnitzer S A amp Bongers F (2011) Increasing liana abundanceand biomass in tropical forests Emerging patterns and pu-tative mechanisms Ecology Letters 14 397ndash406 httpsdoiorg101111j1461-0248201101590x

Schnitzer S Bongers FampWright S J (2011) Community and eco-system ramifications of increasing lianas in neotropical forestsPlant Signaling and Behavior 6 598ndash600 httpsdoiorg104161psb6415373

SchnitzerSAampCarsonWP(2001)TreefallgapsandthemaintenanceofspeciesdiversityinatropicalforestEcology82913ndash919httpsdoiorg1018900012-9658(2001)082[0913TGATMO]20CO2

SchnitzerSAampCarsonWP(2010)Lianassuppresstreeregenerationanddiversity in treefallgapsEcology Letters13849ndash857httpsdoiorg101111j1461-0248201001480x

SchnitzerSADallingJWampCarsonWP(2000)Theimpactoflia-nasontreeregenerationintropicalforestcanopygapsEvidenceforanalternativepathwayofgap-phaseregenerationJournal of Ecology88655ndash666httpsdoiorg101046j1365-2745200000489x

Schnitzer S A DeWalt S J amp Chave J (2006) Censusingand measuring lianas A quantitative comparison of thecommon methods Biotropica 38 581ndash591 httpsdoiorg101111j1744-7429200600187x

Schnitzer S A Kuzee M E amp Bongers F (2005) Disentanglingabove- and below-ground competition between lianas and treesin a tropical forest Journal of Ecology93 1115ndash1125 httpsdoiorg101111j1365-2745200501056x


SchnitzerSARutishauserSampAguilarS(2008)Supplementalpro-tocolforlianacensusesForest Ecology and Management2551044ndash1049httpsdoiorg101016jforeco200710012

SchnitzerSAvanderHeijdenGMFMascaroJampCarsonWP(2014)Lianasingapsreducecarbonaccumulationinatropicalfor-estEcology953008ndash3017httpsdoiorg10189013-17181

SfairJCRochelleALCRezendeAAampMartinsR(2016)Lianaavoidance strategies in trees Combined attributes increase effi-ciencyTropical Ecology57559ndash566

SlikJWFPaoliGMcGuireKAmaral IBarrosoJBastianMhellipZweifelN(2013)Largetreesdriveforestabovegroundbiomassvari-ation inmoist lowland forests across the tropicsGlobal Ecology and Biogeography221261ndash1271httpsdoiorg101111geb12092

StevensGC(1987)LianasasstructuralparasitesTheBursera simaruba exampleEcology6877ndash81httpsdoiorg1023071938806

TabarelliMLopesAVampPeresCA(2008)Edge-effectsdrivetropi-calforestfragmentstowardsanearly-successionalsystemBiotropica40657ndash661httpsdoiorg101111j1744-7429200800454x

TalleySMSetzerWNamp JackesBR (1996)Hostassociationsof two adventitious-root-climbing vines in a north Queenslandtropical rain forest Biotropica 28 356ndash366 httpsdoiorg1023072389199

Terborgh J Lopez LNuntildeez P RaoM ShahabuddinGOrihuelaG hellip Balbas L (2001) Ecological meltdown in predator-free for-est fragments Science 294 1923ndash1926 httpsdoiorg101126science1064397

Tracey JG (1982)The vegetation of the humid tropical region of north QueenslandMelbourneCSIRO

TurtonSM(2012)SecuringlandscaperesiliencetotropicalcyclonesinAustraliarsquosWet Tropics under a changing climate Lessons fromcyclonesLarry(andYasi)Geographical Research5015ndash30httpsdoiorg101111j1745-5871201100724x

TurtonSMampSiegenthalerDT(2004)Immediateimpactsofaseveretropicalcycloneonthemicroclimateofarainforestcanopyinnorth-eastAustraliaJournal of Tropical Ecology20583ndash586httpsdoiorg101017S0266467404001622

Turton S M amp Stork N E (2009) Impacts of tropical cyclones onforests in the Wet Tropics of Australia In N E Stork and S MTurton (Eds) Living in a dynamic tropical forest landscape (pp

47ndash58) MaldenMassachusetts Blackwell Publishing Ltd httpsdoiorg1010029781444300321ch3

TymenBReacutejou-MeacutechainMDallingJWFausetSFeldpauschTRNordenNhellipChaveJ(2015)Evidenceforarrestedsuccessioninaliana-infestedAmazonianforestJournal of Ecology104149ndash159

UNESCO (1988)Decision ndash 12COM XIVA ndash inscription Wet tropics of QueenslandWorldHeritageListParisFranceUNESCO

Wade T G Riitters K H Wickham J D amp Jones K B (2003)DistributionandcausesofglobalforestfragmentationConservation Ecology77httpsdoiorg105751ES-00530-070207

Williams-LineraG(1990)Vegetationstructureandenvironmentalcon-ditionsof forestedges inPanamaJournal of Ecology78356ndash373httpsdoiorg1023072261117

Winter JW Bell F C amp Pahl L I (1987) Rainforest clearfelling innortheasternAustraliaProceedings of the Royal Society of Queensland9841ndash57

Wright S J (2010) The future of tropical forests Annals of the New York Academy of Sciences 1195 1ndash27 httpsdoiorg101111j1749-6632201005455x

WTMA (2009) Vegetation of the wet tropics of Queensland CairnsAustraliaWTMA

ZuurAFIenoENampElphickCS(2010)AprotocolfordataexplorationtoavoidcommonstatisticalproblemsMethods in Ecology and Evolution13ndash14httpsdoiorg101111j2041-210X200900001x

SUPPORTING INFORMATION

Additional Supporting Information may be found online in the supportinginformationtabforthisarticle

How to cite this articleCampbellMJEdwardsWMagrachAetalEdgedisturbancedriveslianaabundanceincreaseandalterationoflianandashhosttreeinteractionsintropicalforestfragmentsEcol Evol 201884237ndash4251 httpsdoiorg101002ece33959


1emsp |emspINTRODUC TION

Habitat fragmentation is globally ubiquitous (Bhagwat 2014RiittersWickhamCostanzaampVogt2016WadeRiittersWickhamamp Jones 2003) In fact it is currently estimated that 70 of theworldrsquosremainingforestiswithin1kmfromaforestedge(Haddadetal2015)This is importantasthefragmentationofforestsandassociatededgeeffectscanreducebiodiversityanddegradeforestfunctioning (eg Fahrig 2003 Laurance Delamonica LauranceVasconcelosampLovejoy2000Lauranceetal20022011MagrachLaurance Larrinaga amp Santamaria 2014a Saunders Hobbs ampMargules1991)Forinstanceforestfragments(32m2ndash100ha)areestimatedtopossess13ndash75lessdiversitythancomparablenon-fragmented forests (Haddad etal 2015)with themajority of thelostdiversityoftenthemost iconiccomponentssuchasbig treesandlargemammals(Chiarello1999Gibsonetal2013Laurance1997bLauranceetal2000OliveiraSantosampTabarelli2008)Inadditionforestfragmentationisalsoknowntoalterordegrademanybeneficialecologicalprocessessuchaspollinationandseeddisper-sal(CampbellLauranceampMagrach2015aCampbellMagrachampLaurance2015bLauranceetal2002Magrachetal2014aPehLinLukeFosterampTurner2014Terborghetal2001)

In the tropics large-scale deforestation has resulted in forestfragmentsnowrepresentingasubstantialproportionoftheremain-ingforestedareainmanyregionssuchastheAtlanticforestofBrazilWestAfricaandtheAthertonTablelandofnortheasternAustralia(Ouedraogo etal 2011 RibeiroMetzgerMartensen Ponzoni ampHirota2009WinterBellampPahl1987)Insuchregionsforestfrag-mentsprovide theprimaryorsole repository for thepreservationofmany rare andendangered species and threatenedecosystems(Arroyo-RodriguezampMandujano2006Arroyo-RodriguezPinedaEscobarampBenitez-Malvido2009Guindon1996)Maximizingtheconservationvalueofforestfragmentsrequiresthatfragmentsarenotonlyretainedbutaremanagedeffectivelywhichnecessitatesanunderstandingoftheirinternalecology

Oneofthemajorecological interactionsalteredbyfragmenta-tion is therelationshipbetweentreesand lianasLianasdetrimen-tally impact trees by limiting seedling recruitment (Schnitzer ampCarson2010SchnitzerDallingampCarson2000)damagingsaplingsanddecreasingtreegrowthandfecundity(Stevens1987)compet-ingwith trees for limited resources (PasquiniWrightamp Santiago2015ReidSchnitzerampPowers2015Rodriacuteguez-RonderosBohrerSanchez-Azofeifa Powers amp Schnitzer 2016 Schnitzer Kuzeeamp Bongers 2005) and increasing tree mortality (IngwellWrightBecklundHubbellampSchnitzer2010)Inadditionlianascanmod-ify the functioning of a forest by reducing carbon storage capac-ity (DuraacutenampGianoli 2013 vanderHeijden Schnitzer PowersampPhillips 2013 Schnitzer van der Heijden Mascaro amp Carson2014) re-distributing nutrients (Kazda 2015 Powers Kalicin ampNewman 2004 SchnitzerampBongers 2011) altering tree-speciescomposition (ClarkampClark1990Lauranceetal2001SchnitzerampBongers2002)threateningepiphyticferns(MagrachRodriacuteguez-PeacuterezCampbellampLaurance2014b)and limitingorchanging the

trajectoryoftree-speciessuccessionwithintreefallgaps(SchnitzerampBongers2005SchnitzerampCarson20012010Schnitzeretal2000)Thus lianascanhavesignificant impactsonboth thebiotaand functioning of remnant forest fragments Understanding theecological interactionsbetween lianasandtheirhost trees iscriti-cal forsuccessfullymanagingremnantforestfragmentsespeciallythosewithhighconservationvalue

There is strong support for theobservation that lianasprefer-entially impact certain ecological ldquoguildsrdquo of tree species such aslate-successionalclimax species (Campbell etal 2015a 2015bClarkampClark1990 Lauranceetal 2001 Schnitzer etal 2000)althoughthereislittleevidencethatthisoccursataspecies-specificlevel (Garrido-Perez amp Burnham 2010 Hegarty 1991 Peacuterez-SalicrupSorkampPutz2001)Theenhanced liana infestationrateson late-successional treespecies is likelyduetotheadvancedage(andthustimeavailableforpossibleinfestation)ofthesetreesandcertain character traits they possess (Hegarty 1991 Schnitzer ampBongers2002)Suchtraitsincludebarkmorphologyandchemicalcomposition (BoomampMori1982Carsten JuolaMaleampCherry2002vanderHeijdenHealeyampPhillips2008Putz1980TalleySetzer amp Jackes 1996) buttresses (Black amp Harper 1979 BoomampMori 1982 Putz 1980) leaf shedding and leaf and stem flexi-bility (Maier 1982 Putz 1984a Rich Lum Munoz amp Quesada1987) treetrellis diameter (ClarkampClark 1990 Perez-SalicrupampdeMeijere2005Peacuterez-Salicrupetal2001Putz1984b) spines(Maier1982Putz1984aRichetal1987)lianandashhostdistanceandavailability (Arroyo-Rodriguez amp Toledo-Aceves 2009 Campbelletal 2017 Muthuramkumar etal 2006 Roeder Slik HarrisonPaudel amp Tomlinson 2015) and synergisms among these traits(SfairRochelleRezendeampMartins2016)Assuchacomparativeassessmentofthepredominanttreetraitsbetweenintactandfrag-mentedforestsandtheirassociationwithlianainfestationmaybeofuseas aproxy todeterminehow forest fragmentation impactslianandashtreeinteractionsandcontributestoincreasedlianaabundancewithinfragmentedforests(Lauranceetal2001)

Thetotalabundanceof lianasisknowntobepositivelyasso-ciatedwithforestedgesandareasofdisturbance(Lauranceetal2001 2014b Ledo amp Schnitzer 2014 Magrach etal 2014bMohandass Campbell Hughes Mammides amp Davidar 2017Mohandass Hughes Campbell amp Davidar 2014 Putz 1984b)High lianaabundancesat forestedgesare likelydue toedgeef-fects (eg Harper etal 2005 Laurance etal 2002 Magnagoetal 2016 Murcia 1995 Williams-Linera 1990) in particularto the increased availability of climbing trellises (ie smaller-stemmedtreesBalfourampBond1993ChittibabuampParthasarathy2001 Londre amp Schnitzer 2006 Putz 1984b Williams-Linera1990)Moreoverforestedgesareoftenmoredisturbedthanfor-estinteriors(Lauranceetal199720112018MagnagoRochaMeyerMartinsampMeira-Neto2015)resultinginincreaseddesic-cationandlightlevelsTheseconditionspreferentiallyfavorlianasover trees throughmechanisms suchasdifferential recruitmentsuccess and resource-interception capacity (Andrade MeinzerGoldsteinampSchnitzer2005Chenetal2015LedoampSchnitzer




























1)

0234 0102 2286 022




0202 0064 3114 001

Canopycover 0216 0091 2364 018






























3emsp |emspRESULTS


















Intercept 2839 0186 1525 lt001




1)

0499 0116 427 lt001


0427 0202 211 035



Altitude 0156 0092 170 089

Fallenlogs 0156 0078 201 044

Canopycover 0246 0142 173 083


0520 0164 316 001












Intercept 0542 0026 2056 lt001

















Treeinfested 1 220284 118 2785166 lt001

Foresttype 1 17823 117 2767343 lt001

Edge 4 32012 113 2735331 lt001

Barktype 2 2549900 110 184913 lt001



Buttressbark 2 11811 81 111681 003













Forest 1 12064 138 3031484 lt001

Guild 6 1032740 132 1998744 lt001

Edge 4 679871 128 1318874 lt001


Forestguild 6 95485 121 1147607 lt001

Forestedge 4 97822 117 1049785 lt001

Guildedge 24 341774 93 708012 lt001






6 22505 52 78981 lt001


24 42878 28 36103 010











ACKNOWLEDG MENTS



Nonedeclared

AUTHOR CONTRIBUTION


ORCID


R E FE R E N C E S








































































































































































1)

0234 0102 2286 022




0202 0064 3114 001

Canopycover 0216 0091 2364 018






























3emsp |emspRESULTS


















Intercept 2839 0186 1525 lt001




1)

0499 0116 427 lt001


0427 0202 211 035



Altitude 0156 0092 170 089

Fallenlogs 0156 0078 201 044

Canopycover 0246 0142 173 083


0520 0164 316 001












Intercept 0542 0026 2056 lt001

















Treeinfested 1 220284 118 2785166 lt001

Foresttype 1 17823 117 2767343 lt001

Edge 4 32012 113 2735331 lt001

Barktype 2 2549900 110 184913 lt001



Buttressbark 2 11811 81 111681 003













Forest 1 12064 138 3031484 lt001

Guild 6 1032740 132 1998744 lt001

Edge 4 679871 128 1318874 lt001


Forestguild 6 95485 121 1147607 lt001

Forestedge 4 97822 117 1049785 lt001

Guildedge 24 341774 93 708012 lt001






6 22505 52 78981 lt001


24 42878 28 36103 010











ACKNOWLEDG MENTS



Nonedeclared

AUTHOR CONTRIBUTION


ORCID


R E FE R E N C E S






























































































































































1)

0234 0102 2286 022




0202 0064 3114 001

Canopycover 0216 0091 2364 018






























3emsp |emspRESULTS


















Intercept 2839 0186 1525 lt001




1)

0499 0116 427 lt001


0427 0202 211 035



Altitude 0156 0092 170 089

Fallenlogs 0156 0078 201 044

Canopycover 0246 0142 173 083


0520 0164 316 001












Intercept 0542 0026 2056 lt001

















Treeinfested 1 220284 118 2785166 lt001

Foresttype 1 17823 117 2767343 lt001

Edge 4 32012 113 2735331 lt001

Barktype 2 2549900 110 184913 lt001



Buttressbark 2 11811 81 111681 003













Forest 1 12064 138 3031484 lt001

Guild 6 1032740 132 1998744 lt001

Edge 4 679871 128 1318874 lt001


Forestguild 6 95485 121 1147607 lt001

Forestedge 4 97822 117 1049785 lt001

Guildedge 24 341774 93 708012 lt001






6 22505 52 78981 lt001


24 42878 28 36103 010











ACKNOWLEDG MENTS



Nonedeclared

AUTHOR CONTRIBUTION


ORCID


R E FE R E N C E S








































































































































































3emsp |emspRESULTS


















Intercept 2839 0186 1525 lt001




1)

0499 0116 427 lt001


0427 0202 211 035



Altitude 0156 0092 170 089

Fallenlogs 0156 0078 201 044

Canopycover 0246 0142 173 083


0520 0164 316 001












Intercept 0542 0026 2056 lt001

















Treeinfested 1 220284 118 2785166 lt001

Foresttype 1 17823 117 2767343 lt001

Edge 4 32012 113 2735331 lt001

Barktype 2 2549900 110 184913 lt001



Buttressbark 2 11811 81 111681 003













Forest 1 12064 138 3031484 lt001

Guild 6 1032740 132 1998744 lt001

Edge 4 679871 128 1318874 lt001


Forestguild 6 95485 121 1147607 lt001

Forestedge 4 97822 117 1049785 lt001

Guildedge 24 341774 93 708012 lt001






6 22505 52 78981 lt001


24 42878 28 36103 010











ACKNOWLEDG MENTS



Nonedeclared

AUTHOR CONTRIBUTION


ORCID


R E FE R E N C E S






















































































































































3emsp |emspRESULTS


















Intercept 2839 0186 1525 lt001




1)

0499 0116 427 lt001


0427 0202 211 035



Altitude 0156 0092 170 089

Fallenlogs 0156 0078 201 044

Canopycover 0246 0142 173 083


0520 0164 316 001












Intercept 0542 0026 2056 lt001

















Treeinfested 1 220284 118 2785166 lt001

Foresttype 1 17823 117 2767343 lt001

Edge 4 32012 113 2735331 lt001

Barktype 2 2549900 110 184913 lt001



Buttressbark 2 11811 81 111681 003













Forest 1 12064 138 3031484 lt001

Guild 6 1032740 132 1998744 lt001

Edge 4 679871 128 1318874 lt001


Forestguild 6 95485 121 1147607 lt001

Forestedge 4 97822 117 1049785 lt001

Guildedge 24 341774 93 708012 lt001






6 22505 52 78981 lt001


24 42878 28 36103 010











ACKNOWLEDG MENTS



Nonedeclared

AUTHOR CONTRIBUTION


ORCID


R E FE R E N C E S






















































































































































Intercept 2839 0186 1525 lt001




1)

0499 0116 427 lt001


0427 0202 211 035



Altitude 0156 0092 170 089

Fallenlogs 0156 0078 201 044

Canopycover 0246 0142 173 083


0520 0164 316 001












Intercept 0542 0026 2056 lt001

















Treeinfested 1 220284 118 2785166 lt001

Foresttype 1 17823 117 2767343 lt001

Edge 4 32012 113 2735331 lt001

Barktype 2 2549900 110 184913 lt001



Buttressbark 2 11811 81 111681 003













Forest 1 12064 138 3031484 lt001

Guild 6 1032740 132 1998744 lt001

Edge 4 679871 128 1318874 lt001


Forestguild 6 95485 121 1147607 lt001

Forestedge 4 97822 117 1049785 lt001

Guildedge 24 341774 93 708012 lt001






6 22505 52 78981 lt001


24 42878 28 36103 010











ACKNOWLEDG MENTS



Nonedeclared

AUTHOR CONTRIBUTION


ORCID


R E FE R E N C E S























































































































































Intercept 0542 0026 2056 lt001

















Treeinfested 1 220284 118 2785166 lt001

Foresttype 1 17823 117 2767343 lt001

Edge 4 32012 113 2735331 lt001

Barktype 2 2549900 110 184913 lt001



Buttressbark 2 11811 81 111681 003













Forest 1 12064 138 3031484 lt001

Guild 6 1032740 132 1998744 lt001

Edge 4 679871 128 1318874 lt001


Forestguild 6 95485 121 1147607 lt001

Forestedge 4 97822 117 1049785 lt001

Guildedge 24 341774 93 708012 lt001






6 22505 52 78981 lt001


24 42878 28 36103 010











ACKNOWLEDG MENTS



Nonedeclared

AUTHOR CONTRIBUTION


ORCID


R E FE R E N C E S






















































































































































Treeinfested 1 220284 118 2785166 lt001

Foresttype 1 17823 117 2767343 lt001

Edge 4 32012 113 2735331 lt001

Barktype 2 2549900 110 184913 lt001



Buttressbark 2 11811 81 111681 003













Forest 1 12064 138 3031484 lt001

Guild 6 1032740 132 1998744 lt001

Edge 4 679871 128 1318874 lt001


Forestguild 6 95485 121 1147607 lt001

Forestedge 4 97822 117 1049785 lt001

Guildedge 24 341774 93 708012 lt001






6 22505 52 78981 lt001


24 42878 28 36103 010











ACKNOWLEDG MENTS



Nonedeclared

AUTHOR CONTRIBUTION


ORCID


R E FE R E N C E S






















































































































































Forest 1 12064 138 3031484 lt001

Guild 6 1032740 132 1998744 lt001

Edge 4 679871 128 1318874 lt001


Forestguild 6 95485 121 1147607 lt001

Forestedge 4 97822 117 1049785 lt001

Guildedge 24 341774 93 708012 lt001






6 22505 52 78981 lt001


24 42878 28 36103 010











ACKNOWLEDG MENTS



Nonedeclared

AUTHOR CONTRIBUTION


ORCID


R E FE R E N C E S





















































































































































ACKNOWLEDG MENTS



Nonedeclared

AUTHOR CONTRIBUTION


ORCID


R E FE R E N C E S
















































































































































































































































































































































































































































































Documents

Edge disturbance drives liana abundance increase and ... Campbell...tion of forest succession, and a substantial decline in forest carbon storage. We ex-amined the individual impacts