multiple stages of tree seedling recruitment are altered ...€¦ · tropical forest degradation is...
TRANSCRIPT
Ecology and Evolution 201888231ndash8242 emsp|emsp8231wwwecolevolorg
Received15January2018emsp |emsp Revised12March2018emsp |emsp Accepted14May2018DOI 101002ece34352
O R I G I N A L R E S E A R C H
Multiple stages of tree seedling recruitment are altered in tropical forests degraded by selective logging
Rajeev Pillay1 emsp|emspFangyuan Hua2emsp|emspBette A Loiselle13emsp|emspHenry Bernard4emsp|emsp Robert J Fletcher Jr1
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsEcology and EvolutionpublishedbyJohnWileyampSonsLtd
1DepartmentofWildlifeEcologyandConservationUniversityofFloridaGainesvilleFloridaUSA2DepartmentofZoologyUniversityofCambridgeCambridgeUK3CenterforLatinAmericanStudiesUniversityofFloridaGainesvilleFloridaUSA4InstituteforTropicalBiologyandConservationUniversitiMalaysiaSabahKotaKinabaluSabahMalaysia
CorrespondenceRajeevPillayDepartmentofWildlifeEcologyandConservationUniversityofFloridaGainesvilleFloridaUSAEmailrajeevp20agmailcom
Funding informationRuffordSmallGrantsFoundationInstituteofFoodandAgriculturalSciencesTropicalConservationandDevelopmentProgramUniversityofFloridaIDEAWild
AbstractTropical forest degradation is a global environmental issue In degraded forestsseedlingrecruitmentofcanopytreesisvitalforforestregenerationandrecoveryWeinvestigatedhowselectiveloggingapervasivedriveroftropicalforestdegradationimpacts canopy tree seedling recruitment focusing on an endemic dipterocarpDryobalanops lanceolatainSabahBorneoDuringamast-fruitingeventinintensivelyloggedandnearbyunloggedforestweexaminedfourstagesoftheseedlingrecruit-ment process seed production seed predation and negative density-dependentgerminationandseedlingsurvivalOurresultssuggestthateachstageoftheseedlingrecruitmentprocessisalteredinloggedforestTheseedcropofD lanceolatatreesinloggedforestwasone-thirdsmallerthanthatproducedbytreesinunloggedforestThefunctionalroleofvertebratesinseedpredationincreasedinloggedforestwhilethatofnon-vertebratesdeclinedSeedsinloggedforestwerelesslikelytogerminatethan those in unlogged forestGermination increasedwith local-scale conspecificseeddensity inunloggedforestbutseedlingsurvivaltendedtodeclineHoweverbothgerminationandseedlingsurvival increasedwith local-scaleconspecificseeddensityinloggedforestNotablyseedcropsizegerminationandseedlingsurvivaltendedtoincreaseforlargertreesinbothunloggedandloggedforestssuggestingthat sustainable timberextractionand silviculturalpracticesdesigned tominimizedamagetotheresidualstandareimportanttopreventseedlingrecruitmentfailureOveralltheseimpactssustainedbyseveralaspectsofseedlingrecruitmentinamast-fruitingyearsuggestthatintensiveselectiveloggingmayaffectlong-termpopulationdynamicsofD lanceolata It isnecessary toestablish ifotherdipterocarpspeciesmanyofwhicharethreatenedbythetimbertradearesimilarlyaffectedintropicalforestsdegradedbyintensiveselectivelogging
K E Y W O R D S
BorneoDryobalanops lanceolatagerminationmast-fruitingnegativedensity-dependenceseedpredationseedproductionseedlingsurvivalsurvivalanalysis
8232emsp |emsp emspensp PILLAY et AL
1emsp |emspINTRODUC TION
Vastareasofnatural forestarebeingdegradedaroundtheworldInthetropicsselectiveloggingcharacterizedbyunsustainablehar-vest rates and improper silvicultural practices is amajor driver offorestdegradation (AsnerRudelAideDefriesampEmerson2009MartinNewtonPfeiferKhooampBullock2015Putzetal2012)Theconsensusofrecentinsightsintohowselectivelogging(hereaf-terldquologgingrdquo)affectsbiodiversityisthatmostspeciesacrosstaxo-nomicgroupsappeartopersistinloggedforests(EdwardsTobiasSheilMeijaardampLaurance2014Putzetal2012WilcoveGiamEdwards Fisher amp Koh 2013)What remains poorly understoodhoweverishowloggingmayaffectnumerousecologicalprocessesthatarethefoundationofecosystemfunctioningandmaintenance(Ewersetal2015Schleuningetal2011)Seedlingrecruitmentisamongthefundamentalprocessesthatdeterminethemaintenanceofplantdiversityinforestecosystems(Wright2002)andisade-mographic bottleneck in plant population dynamics (Chambers ampMacMahon1994Chesson2000PoulsenClarkampBolker2012)In theaftermathofdisturbances suchas logging seedling recruit-mentofcanopytrees isvital for forest regenerationandrecovery(Bagchi etal 2011 Chazdon 2003) Despite its importance ourknowledgeoftheimpactofloggingonseedlingrecruitmentislim-ited(Bagchietal2011Curranetal1999)
There are several pathways by which logging may impactseedling recruitment First the removal of the largest andmostreproductively active trees (Fisher etal 2011) may directly re-ducetotalseedproductionatthescaleofthe landscape (Bagchietal 2011)The remaining treesmayalsobecomespatially iso-lated from reproductive conspecifics which may reduce cross-pollinationandindirectlydecreaseseedcropsizeatthescaleofindividualtrees(GhazoulListonampBoyle1998MurawskiNimalGunatillekeampBawa1994)Secondthespatial isolationofadulttrees from conspecifics in logged forestsmay concentrate seedpredatorsatthesetrees(Bagchietal2011)potentiallyincreasingthe strengthofpredator-mediatednegativedensity-dependence(NDD)aprocessthatunderliesseedlingrecruitmentbeyondtheseed production stage (Bagchi etal 2014 Swamy amp Terborgh2010)NDD or the tendency for seeds and seedlings to exhibitreducedsurvivalwithincreasedconspecificdensityatlocalscalesisapervasivedemographicforcethatmaintainsplantcommunitydiversitybypreventingthedominanceofcommonspecies(Bagchietal 2014 Comita Muller-Landau Aguilar amp Hubbell 2010Connell 1971 Harms Wright Calderoacuten Hernaacutendez amp Herre2000 Janzen 1970WebbampPeart 1999) Third seedpredatorcommunities comprising insects fungal pathogens and verte-brates may undergo population shifts in logged forests (Ewersetal 2015) The functional roles playedby various seedpreda-torsmayalsochange(Ewersetal2015)potentiallyalteringthestrengthofNDDinconstrainingtherecruitmentofcommonspe-cies (Bagchietal2011)Fourthseeds in loggedforestsmaybeexposed to increased light penetration and hotter drier air andsoilconditionsduetotherelativelyopencanopy(Hardwicketal
2015)Theseabioticfactorscannegativelyaffectseedlingrecruit-ment(Bruna1999)Thusmultiplestagesofseedlingrecruitmentmaybealteredinforestsdegradedbylogging
Understandinghowloggingmayimpactvariousstagesofseed-lingrecruitmentisaparticularlyrelevantissueinthedipterocarp-dominated (Family Dipterocarpaceae) tropical rainforests ofSoutheastAsiaNot only is this ecosystem imperiled by logging(Asner etal 2009) but its unique mast-fruiting ecology alsolikelyrenders itsseedlingrecruitmentprocesstoresponddiffer-ently to loggingcomparedwithother tropical forestecosystems(Bagchietal2011)Mast-fruiting inSoutheastAsianrainforestsoccursapproximatelyevery3ndash9years (Janzen1974)andistypi-callycommunitywideupto88ofcanopytreespeciesmayfruitsynchronously (Curran amp Leighton 2000 Curran etal 1999)For dipterocarps many species of which are targets of logging(SoepadmoSawampChung2002SoepadmoampWong1995)mast-fruiting years account for the majority of seedling recruitment(CurranampLeighton2000Janzen1974)Impactsondipterocarpseedling recruitment during mast-fruiting years may thereforehavedisproportionatelyimportantconsequencesfortherecoveryofloggedforestsinSoutheastAsia(Bagchietal2011CurranampLeighton2000)WhileitisknownthatdipterocarpsmayundergorecruitmentfailureinloggedforestsofSoutheastAsiaduringnon-mast years (Bagchi etal 2011) empirical understandingofhowvarious stages of seedling recruitment are impacted by loggingduring mast-fruiting years is limited (Curran amp Leighton 2000CurranampWebb2000)
Herewe investigate the impactof loggingon theseedling re-cruitment process of an endemic and endangered dipterocarpspeciesheavily targetedby loggingDryobalanops lanceolataBurck(Ashton 1998) during a mast-fruiting event in Sabah BorneoWe combined natural observations and an exclosure experimentoveronemast-fruitingseasontotestthefollowingpredictions (1)Loggingremovesthe largestmostreproductivelyactivetreesandmayincreasethespatialisolationoftheremainingtreesrelativetoeachotherThereforeweexpectedtheseedcropwouldbesmallerin logged forest than in unlogged forest (2) Vertebrate and non-vertebrate seed predator communities in logged forests may un-dergopopulationincreasesanddeclinesrespectively(Ewersetal2015)Consequentlyweexpectedthefunctionalroleofvertebratesin seed predation to increase and that of non-vertebrates to de-creaseinloggedforest(3)Althoughthehighseeddensitiestypicalof SoutheastAsianmast-fruiting forests usually reduce seedmor-talitybysatiatingpredators(Janzen19701974)wepredictedtheconcentratedseeddensitiesunderspatiallyisolatedtreesinloggedforestsmayallowNDDtooperate(Bagchietal2011)Thereforewe expected the relationship between seedling recruitment andlocal-scale conspecific seed density would be stronger in loggedforestthaninunloggedforestWefocusedontheseed-to-seedlingtransitionphaseover3monthsafterseedfallademographicbottle-neckthatdisproportionatelyinfluencesthestructuredynamicsandcomposition of tree communities (Chambers ampMacMahon 1994Chesson2000Poulsenetal2012)
emspensp emsp | emsp8233PILLAY et AL
2emsp |emspMATERIAL S AND METHODS
21emsp|emspStudy area
Weconductedfieldworkintwodipterocarp-dominatedforestsitesspaced 65km apart in Sabah Malaysian Borneo These sites arepart of the experimental design of the Stability of Altered ForestEcosystems(SAFE)Project(Ewersetal2011)andencompasspri-maryforestwithintheMaliauBasinConservationArea(MBCA)andrepeatedlyloggedforestwithintheKalabakanForestReserve(KFR)aloggingconcessionintheYayasanSabahForestManagementAreaOverallthelogginggradientencompassedwithintheSAFEexperi-mental design resembles the pattern of habitat conversion acrossthewiderregion(Ewersetal2011Struebigetal2013)
TheforestatMBCA(a5884km2protectedarea)representsthenearest topographicallymatchedprimary forest to the logged for-est inKFR(Ewersetal2011Struebigetal2013)Thetwositesarealsosimilar intermsofsoilnutrientprofilesandphysicalprop-erties(Riuttaetal2018)TheMBCAservesastheunloggedcon-trolsiteof theSAFEProject (Ewersetal2011)Twoof thethreecontrolblocks atMBCA (hereafter ldquounlogged forestrdquo) (OG1OG2)haveneverbeenloggedwhilethethird(OG3)waslightlyloggedinthe1970sand1990s (seeEwersetal2011)AspartoftheSAFEProjectexperimentalforestfragments(110100ha)arebeingcre-atedinKFR(Ewersetal2011)PriortothisexperimentKFRwassubjectedtomultiplerotationsofloggingthefirstofwhichbeganinthe1970s(Chong2005Fisheretal2011)Commerciallyvalu-abletreesgt60cmdiameteratbreastheight(DBH)wereextractedand11296m3haoftimberwasremoved(Fisheretal2011)Thesecond rotation commencing in the 2000s (Chong 2005 Fisheretal2011)encompassedthreeroundsduringwhichtreesgt40cmDBH were targeted (Fisher etal 2011 Struebig etal 2013) Avolumeof25872232 and1816m3haof timberwasextractedduringeachroundrespectively(YayasanSabahunpublisheddata)Logging ended in 2007ndash2008 (Fisher etal 2011) by which time17931m3haof timberwascumulatively removed (Struebigetal
2013)Extensivecollateraldamagetoforeststructurealsooccurredduetotheestablishmentofskidtrailsaccessroadsandlog-landingareas (WearnRowcliffeCarboneBernardampEwers2013)Thustheloggingintensitywasaround45timesthethresholdoflt40m3habeyondwhichresidualstanddamagesurpassesthe25ndash30limitconsidered sustainable (Martin etal 2015) The six experimentalblocks(AndashF)atSAFE(hereafterldquologgedforestrdquo)(Ewersetal2011)comprise a heterogeneous landscape that has been subjected tovaryingintensitiesandtimingsoftimberextraction
22emsp|emspStudy species
Dryobalanops lanceolataBurckisanemergenttreethatcangrowupto80mhigh(Soepadmoetal2002)EndemictoBorneoitiswide-spread and common in the statesof Sabah andSarawak growinginmixed-dipterocarp forestonclay-richsoils (SoepadmoampWong1995Soepadmoetal2002)Thesaplingsareshadetolerant(ItohYamakuraOginoampLee1995)andcansurvivemanyyearsexpand-inghorizontallyuntilacanopygapopensup(Soepadmoetal2002)It is ahardwoodspeciesvalued for its construction timber that issoldunder the tradenameKapur (Soepadmoetal 2002)Due tocommercialharvestingandhabitat loss it isnowrareoutsidepro-tectedareasand isclassifiedasEndangered(IUCNRedListv23Ashton 1998) Like other dipterocarps its winged seeds are dis-persedbygyration (Figure1)andmostly fall incloseproximity tothecrownoftheparenttree(ItohYamakuraOginoLeeampAshton1997)Itsseedsandseedlingsareattackedbyfungalpathogens(per-sonal observation)insectsandvertebratessuchasbeardedpigs(Sus barbatus)andvariousspeciesofrodents(Itohetal1995)
23emsp|emspStudy design
Weconductedfieldworkduringamast-fruitingeventthatoccurredin2014 InJuneandJulyprior to thecommencementofseedfallwe surveyed ~2146km of forest trails that passed through thediametersof the110 and100ha ldquofragmentsrdquoofBlocksABD
F IGURE 1emspDryobalanops lanceolataisanendangereddipterocarpendemictoBorneoTheseedsarewinddispersedandmostlyfallneartheparenttreeLeftAmatureseedgerminatingD lanceolataseedshavefivewingsandaregreenwhentheyfallfromthetreebutturnpinkupongerminationwithin5ndash7daysofdispersalCenterMarkedseedlingsinanaturalplotRightSeedlingsinanexperimental(vertebrateexclosure)plotPhotocreditsRajeevPillay
8234emsp |emsp emspensp PILLAY et AL
E andF in the logged forest andwere able to locate only sevenadultD lanceolatatreesinactivefruitingcondition(withinBlockEtwotreeswithinandaroundBlockFfivetrees)OneofthetreesinBlockEwaslt40mfromtheotherreproductiveconspecificWeremovedthis individual fromthisstudytoensurenon-overlappingseedshadowssincepriorworkonD lanceolatainSarawakBorneo(Itohetal1997)indicatesthatallseedsaredispersedlt40mfromthe parent treeWe included the remaining six individuals in thisstudyThusthesparsenumberofadultconspecificsinactivefruit-ingconditiondictatedoursamplesizeatthelevelofindividualtreesIn the unlogged forest sitewe surveyed approximately 65kmofforesttrailseachinBlocksOG1andOG2andlocated15ndash20(OG1)and20ndash25(OG2)adultD lanceolatatreesinactivefruitingcondition(weexcludedOG3fromthisstudydueto its logginghistory)TheseedshadowsofalltreesinOG1overlappedwiththoseofatleastoneotherconspecificadultThereforeweselectedsevenindividu-alsinOG2whoseseedshadowsdidnotoverlapwiththoseofotherreproductiveconspecificsWeconsideredeachindividualfocaltreeasanexperimentalunitresultinginsevenandsixreplicatesatthelevelofindividualtreesinunloggedandloggedforestrespectivelyIndividualtreesareoftenusedasexperimentalunitsinseeddisper-salandseedlingrecruitmentstudiesandmaybeconsidered inde-pendentsamplesiftheirseedshadowsdonotoverlapwiththoseofotherconspecifics (Bagchietal2011HolbrookampLoiselle2009Poulsenetal2012)
Thesevenfocaltreesinunloggedforestwere303mapartonaveragewith the smallest pairwise distance between two treesbeing40mThesixfocaltreesinloggedforestwere1690mapartonaveragewiththesmallestpairwisedistancebetweentwotreesbeing244mandcoverconsiderable landscapeheterogeneity interms of logging intensity and time since logging (Wearn etal2013)Onaverageourfocaltreeswerearound56timesfurtherapart from each other in logged forest than in unlogged forestwhichpotentiallyindicatestheintensityofextractionifD lance-olatapopulationdensitiesweresimilar inbothforesttypespriortologging
Wesetupfour32mtransectsextendingfromthebaseofeachfocaltreewiththefirsttransectorientedalongarandomcompassdirection and each subsequent transect at 90deg from the previous(Figure2)We constrained transect length to 32m because priorwork indicated that few seeds reached this distance (Itoh etal1997)AlongeachtransectweusedseedtrapstoquantifytheseedcropandseeddispersaldistancesettingthemupsoonafterseedfallcommencedinearlyAugust2014Wedeployedtheseedtrapsonalog2scaleat124816and32mdistances(n=24seedtrapstreeFigure2)Eachtrapwasa1times1mnylonmeshnetsuspendedby1-mtallPVCpipesateachcornerThevalidityofourdatareliesontheassumptionthatourfocaltreeshadnon-overlappingseedshadowsSince995of all seeds fell into the seed trapswithin16m fromtheirrespectiveparenttrees(seeSection3)adistancethat is lessthanhalfoftheminimumdistancebetweenanyofourfocal trees(ie40m)theseedsweincludedinthisstudyshouldbepredomi-nantlyifnotentirelyfromtheirrespectiveparenttrees
Wemonitoredseedpredationanddensity-dependentpatternsofgerminationandseedlingsurvivalof individualseedsthatnatu-rally dispersed into individual 1times1m unmanipulated monitoringplots (hereafter ldquonatural plotsrdquo) We thus utilized the conspecificseedseedlingdensitygradientnaturallygeneratedbythedistancegradient forourassessmentofNDDWeplacednaturalplots2mtotheleftoftheseedtrapsalongeachtransectat24816and32m distances (n=20 natural plotstree Figure2) Additionallyaround 1month after the commencement of seedfall we set upvertebrate-exclosure plots (hereafter ldquoexperimental plotsrdquo) andpairednon-exclosureplots(hereafterldquocontrolplotsrdquo)totestfortherelativecontributionofvertebratesversusinsectsandfungitoseedpredationWeplacedexperimentalandcontrolplotsat2and32mdistancesalongone randomlyselected transectateach focal tree(n=2 plot pairstree Figure2)At 32mweplaced eachplot pair2mfromeachotherandontherightsideofthecorrespondingseedtraprandomlyassigningtherelativepositionofexperimentalversuscontrolplots(iewhichplotwasplacedadjacenttothecorrespond-ingseedtrap)At2mduetolimitedspacenearthebaseofthefocaltreeweplacedoneplotontherightofthecorrespondingseedtrapandthepairedplotatthecorrespondingpositionalongthediago-nallyoppositetransectrandomlyassigningtherelativepositionofexperimentalversuscontrolplots (Figure2)Dueto logisticalcon-straintsweomittedoneof themost remote focal trees in loggedforestinthiscomparisonandinsteadsetuptwoadditionalplotpairsinthesamewayaroundanotherofourfocaltreeswhichwasmore
F IGURE 2emspStudydesignshowingseedtraps(at124816and32mdistances)naturalplots(at24816and32mdistances)andpairedexperimental(vertebrateexclosures)andcontrolplots(at2and32mdistances)alongfour-32mtransectsfromthebaseoffocalD lanceolatatreesSeedtrapsnaturalandcontrolplotswere1times1minareaExperimentalplotswere1times1times05mFigurenottoscale
12 4 8 16 32
Focal treeSeed trapNatural plotExperimental plotControl plot
emspensp emsp | emsp8235PILLAY et AL
accessible Experimental plotswere 1times1times05mwith the exclo-suremade fromsteelwireof127times127cmmeshsize toexcludeallvertebrateseedpredatorsbutnotinsectseedpredatorsorfungalpathogens(Figure1)Controlplotswereopentoallseedpredatorsandpathogens
ForthepairedexperimentalandcontrolplotsweaddedD lance-olataseedsatpredefineddensities~1monthaftercommencementof seedfall and thereafter continuously removed all conspecificseedsthatfellintothecontrolplotsthroughoutthedurationofthestudyWeused a seeddensity of 5seedsm2 for thepairedplotsat2mdistancesand50seedsm2 forthoseat32mdistancesForseeding the plots we collected intact (ie no visible evidence ofpredatorattack)matureseedsfromaround20non-focalD lanceo-latatreesinunloggedforestWethoroughlymixedtheseseedsandplacedthemonthesoilsurfaceinaregulargridtomimicthenaturalseedfallpatterninwhichseedsgyratefromtheparenttreesandlandonthegroundWethusdistributed770seeds(n=28experimentalandpairedcontrolplots)ineachforesttypeWenotethatthispartofthestudyaimstoprovideonlyasupportingassessmentoftherel-ative importanceofvertebrateandnon-vertebrateseedpredatorsinunloggedandloggedforestsWedidnotattempttomanipulatedensity anddistance independentlydue to logisticaldifficulties incollecting and sowing additional seeds a time-sensitive undertak-ingbecauseoftherapidityatwhichseedsgerminatetogenerateaspectrumofseeddensities thatwouldreflectscenariosunderun-loggedandloggedconditions(cfBagchietal2011Poulsenetal2012)
24emsp|emspData collection
We collected seeds from the traps at two census intervals be-tween12Augustand4Novemberinloggedforestandbetween1Septemberand22October inunloggedforestWemonitoredthefateofeveryseeduponinitiatingthenaturalplots(atthesameinter-valsastheseedtraps)untiltheendofthestudyWetaggedallseedswithnumberedplastictagsstapledtotheirwings(Figure1)andcon-tinuedtaggingseedsthatnewlyfell intothenaturalplotsAteachcensusintervalwerecordedthenumberofseedsthatsurvivedanddiedineachplotForsurvivingseedswerecordediftheywereger-minatingandsubsequentlywhether they recruited into seedlingsWealsoscoredeachseedintooneofthefollowingcategories(afterBagchietal2011)intact(novisiblesignsoffungalinsectorverte-brateattack)germinated(definedasemergenceoftheradicleItohetal1995)seedling(ge5cmtallexpandedtrueleaves)vertebratedepredated(partiallyeatengnawedorremoved)insectdepredated(withentryexitholes) fungusdepredated(withfungalsporesmy-celia)Wenote that the seeds falling into the natural plotswouldlikely be exposed to both pre-dispersal and postdispersal insectpredators(Bagchietal2011)Wewerecarefultoclassifydepreda-tionstatusonthebasisofthepredatorthatweinitiallyrecordedtohaveattackedtheseedseedling(LewisampGripenberg2008)Thusaseedwithinsectentryexitholesattheinitialcensusthatwassub-sequentlypartiallyeatenorremovedbyvertebrateswasscoredas
predatedbyinsectsDuetothedifficultyinascertainingtheinitialpredatorbetweeninsectsandfungalpathogenswecollapsedthemintothenon-vertebratecategoryWethususedtwopredatorcat-egoriesvertebrateversusnon-vertebrate
WemeasuredasetofecologicalcovariatesthatcanpotentiallyinfluencevariousstagesofseedlingrecruitmentandthusshouldbeaccountedforinexaminingtheimpactsofloggingThesecovariatesincludedthreemeasuresoftreesizethataredeterminantsofseedcropsizeanddispersaldistanceDBHheightandcrowndiameter(CousensDythamampLaw2008NorghauerNockampGrogan2011)We also measured percentage canopy cover as a proxy for lightavailabilitywhich in turnmay influencegerminationand seedlingsurvival(Kobe1999)SeeSupportinginformationAppendixS1fordetailsonthesemeasurements
25emsp|emspStatistical analyses
Wefirstusedprincipal-componentsanalysis(PCA)toidentifymajortrends intreesizedataandreducethenumberofvariablesrepre-sentingtreesizeThefirstprincipalcomponent(PC1)waspositivelycorrelatedwithallthreevariablesrepresentingtreesizehadanei-genvaluegt1andexplained764ofthetotalvarianceintreesizedata (Supporting information Table S1) We used the componentscoresgeneratedfromthe loadingsofPC1asasurrogatefor treesizeinfurtherstatisticalanalyses
Wethenusedgeneralizedlinearmixedmodels(GLMMs)toana-lyzetheimpactsofloggingonseedcropsizeanddispersalpatternsusingthenumberofseeds ineachseedtrapastheresponsevari-ableWeusedforesttype(unloggedvslogged)distancefromthefocaltreePC1(hereafterldquotreesizerdquo)andalltwo-wayinteractionsbetween forest type and the other variables as fixed effectsWeincluded individualseedtrapsnestedwithintreesasa random in-terceptinallmodelsWeassumedaPoissonerrordistributionandaloglinkfunctionWetestedforoverdispersionbycalculatingthesumofsquaredPearsonresidualsandcomparing it totheresidualdegreesoffreedomforeachmodel(ZuurIenoWalkerSavelievampSmith2009)
WealsousedGLMMstoanalyzetheimpactofloggingontherelative role of vertebrates versus non-vertebrates inD lanceo-lataseedandseedlingpredationOurobservationsindicatedthatmostseedlingsdiedfrompredation(eguprootedandpartiallycompletelyconsumedremovedbyvertebratescotyledonsofger-minatedseedlingsdestroyedbyinsectsandorfungalpathogens)rather than from leaf damage typically inflicted by herbivores(ColeyampBarone1996)Thereforewepooleddataon seedandseedling predation For the natural plotswe scored each seedseedling as depredated by either vertebrate or non-vertebratepredators and then modeled the probability of a seedseedlingbeingdepredatedbyvertebrates (relative tonon-vertebrates)asa functionof forest typeas the fixedeffectvariableForpairedexperimental and controlplotswecounted thenumberofdep-redated seedsseedlings out of the total number of seeds andthenmodeledtheprobabilityofseedseedlingpredationWeused
8236emsp |emsp emspensp PILLAY et AL
foresttypeandtreatmenttype(experimentalvscontrolplots)asfixedeffectvariablesInbothanalysesofseedseedlingpredationweincludedindividualplotssequentiallynestedwithintransectsandtreesasarandominterceptWeassumedabinomialerrordis-tribution and a logit link functionWe note that nomadic herdsof bearded pigs destroyed our experimental exclosures for fourout of seven trees in unlogged forest (but not in logged forest)between1and19October(~30daysfromtheonsetofseedseed-lingmonitoringintheseplots)Thereforeforunloggedforestweonly considered data from the paired experimental and controlplotsforthethreetreesthatwerenotdepredatedbybeardedpigs(n=330seeds12plots)
WeusedCoxregressionmixed-effectssurvivalmodelstoan-alyzethe impactof loggingongerminationandseedlingsurvivalatthelevelofindividualseedsandseedlingswithdatacollectedfromthenaturalplotsWefirstmodeledseedsurvivaluntilger-minationwithsurvivalmodeledasdailygerminationrateOftheseeds that germinatedwe subsequentlymodeled daily seedlingsurvivaluntil3monthsafterseedfallWeincorporatedseedseed-lingageandusedright-censoring ifaseedseedlingsurvivedbe-yondtheendofthemonitoringperiodForfixedeffectvariablesweincludedforesttypelocal-scale(1m2)conspecificseedseed-lingdensity (hereafter ldquoconspecificseeddensityrdquo)distancefromthe parent tree and percentage canopy coverWe also includedtree size and total conspecific seedfall at each tree during thestudy (surrogate formedium-scale seed density) as fixed effectvariables because these factorsmay vary between the two for-esttypesandpotentiallyinfluenceseedlingrecruitmentpatterns(Bagchi etal 2011 CurranampWebb 2000) Lastlywe includedinteractions between forest type and the five latter variablesForrandomeffectswesequentiallynestedtheidentitiesofplotswithintransectsandtreestocontrolforpotentialvariationinmi-crotopographythatcouldcausedifferentialgerminationandseed-lingsurvival(Bornetal2015)
Fortheanalysesdescribedabovewebuiltsetsofsub-modelsbasedontheglobalmodelandcomparedmodelsusingAkaikersquos
Information Criterion adjusted for sample size (AICc) (BurnhamampAnderson2002)WeconsideredmodelsfromthelowestAICc until thecumulativemodelweightexceeded95Wethenusedthis95confidencemodelsetasthebasisformodelaveragingandstatisticalinference(BurnhamampAnderson2002)Weconductedall statistical analyses inR (v 321) (RDevelopmentCoreTeam2017)andusedtheglmer function in thepackageldquolme4rdquo (BatesMaumlchler Bolker ampWalker 2015) to fit all GLMMs the packageldquocoxmerdquo(Therneau2015)tofitsurvivalmodelsandthepackageldquoMuMInrdquo(Bartoń2016)formodelselectionandaveraging
3emsp |emspRESULTS
31emsp|emspImpact of logging on seed crop size
ThefivemostparsimoniousmodelswithacumulativeAICcweightof100(Supporting informationTableS2) indicatedthat foresttypedistancefromthefocaltreetreesizeandinteractionsbe-tweenforesttypeandtheothervariableshadsupportinexplain-ingvariationinD lanceolataseedcropsizeanddispersalpatternsConsistentwithprediction1theseedcroptendedtobesmallerin logged forest than in unlogged forest evenwhen accountingfor tree size (Figure3a Table1a)Over ~3months (85days)wecollected2105(n=168traps)and718(n=144traps)seedsinun-loggedandloggedforestrespectivelyTheaverageseeddensity(plusmn1SE) inunloggedforestwas1252(plusmn099)seedsm2comparedwith498(plusmn048)seedsm2inloggedforestThenumberofseedsdeclinedwithincreasingdistancefromthefocaltreesinbothfor-est types (Figure3bTable1a)Consistentwithpatternsof localseed dispersal (Itoh etal 1997) only 06of all trapped seedslanded at 32m in unlogged forest and none in logged forestLarger trees tended toproducemoreseeds inboth forest types(Figure3cTable1a)althoughtreesinloggedforestweresmallerthanthoseinunloggedforest(SupportinginformationFigureS1)Wefoundnoevidenceforoverdispersion(SupportinginformationTableS3)
F IGURE 3emspTherelationshipbetweenD lanceolataseeddensityand(a)foresttype(b)distancefromfocaltreesineachforesttypeand(c)treesizeineachforesttypeErrorbarsandtheshadedregionsofthecurvesarethepredicted95confidenceintervals
(a) (b) (c)
emspensp emsp | emsp8237PILLAY et AL
32emsp|emspImpact of logging on the predation of seeds and seedlings
Over3monthswerecordedanoverallseedandseedlingpredationrate of 866 and 836 in unlogged (n=1423 seeds 140 naturalplots)andlogged(n=646seeds120naturalplots)forestrespec-tivelyAsmallnumberofseeds(unloggedforest5loggedforest8)diedofdesiccationConsistentwithprediction2therewasashiftinthefunctionalroleofseedpredatorsawayfromnon-vertebratesto-wardvertebratesinloggedforest(Figure4ab)Inthenaturalplotsthe log odds of a seedseedling being depredated by vertebrates(relativetonon-vertebrates)werehigherinloggedforestthaninun-loggedforest(βlogged079SE05095CIminus028to185Figure4aSupportinginformationTableS4)Furthersupportingprediction2the logoddsofseedandseedlingpredationwere lower intheex-perimentalexclosureplotsthaninthecontrolplotsinloggedforest(βlogged-exclosureminus210SE05795CIminus343 tominus097Figure4b)In contrast the effect of exclosure treatments on seed predationtendedtobeweakerinunloggedforest(βunlogged-exclosureminus102SE 08895CIminus290to089Figure4bSupportinginformationTableS5)
33emsp|emspImpact of logging on density- dependent germination and seedling survival
We monitored the germination and survival status of seeds thatwerealiveinthenaturalplotsatthefirstcensus(603and227seedsin unlogged and logged forest respectively) until the end of thestudy The sixmost parsimoniousmodelswith a cumulativeAICcweightof97(SupportinginformationTableS6)indicatedthatfor-est type conspecific seed density distance from the parent treeseedfall tree size canopy cover and interactions between foresttypeandtheothervariableshadsupport inexplainingvariation inseedgerminationSeedsfacedgreaterhazard(iehigherprobabilityofmortality) inloggedforestthaninunloggedforest(Table1b)as471ofseedsfailedtogerminateinloggedforestcomparedwith08 in unlogged forestHigher conspecific seed densitywas as-sociatedwithlowerseedmortalityinunloggedforestandthisrela-tionshipalsotendedtoapplyinloggedforest(Figure5aTable1b)With increasingdistancefromparenttreesseedmortalitytendedto increase in both forest types but this relationshipwasweakerin logged forest (Figure5b Table1b) Higher seedfall and largertreesizetendedtobeassociatedwithlowerseedmortalityinbothforest types (Figure5cdTable1b)With increasing canopy coverseedmortality tended to increase inboth forest types (Figure5eTable1b)
Forexplainingvariationinseedlingsurvivalthetwomostparsi-moniousmodelswithacumulativeAICcweightof99(SupportinginformationTableS7) indicated that forest type conspecific seeddensity distance from the parent tree seedfall tree size canopycoverandinteractionsbetweenforesttypeandtheothervariableshad support Of the seeds that germinated seedlings tended tohavelowerprobabilityofmortalityinloggedforestthaninunlogged
forest(Table1c)as817ofgerminatedseedlingssurviveduptotheendofthestudyinloggedforestcomparedwith311inunloggedforestHigherconspecificseedlingdensitytendedtobeassociatedwithhigherseedlingmortality inunloggedforestbut inconsistentwith prediction 3 this relationship was reversed in logged forest(Figure5f Table1c) With increasing distance from parent treesseedlingmortalityincreasedinunloggedforestbutthisrelationshiptendedtobereversedinloggedforest(Figure5gTable1c)Higherseedfall tended tobe associatedwithhigher seedlingmortality inunloggedforestbutthisrelationshipalsotendedtobereversedinloggedforest(Figure5hTable1c)Likegerminationlargertreesizetendedtobeassociatedwithlowerseedlingmortalityinbothforesttypesandthisrelationshipwasstrongerinloggedforest(Figure5iTable1c)With increasingcanopycoverseedlingmortalitytendedtoincreaseinunloggedforestbutthisrelationshiptendedtobere-versedinloggedforest(Figure5jTable1c)
4emsp |emspDISCUSSION
Ourresultsdemonstratehowmultiplestagesoftheseedlingrecruit-mentprocessofacanopytreespeciesmaybealteredwhentropicalforestsaredegradedbyintensiveldquoselectiverdquologgingConsistentwithourpredictions the remaining reproductive trees in logged forestproducedamarkedlysmallerseedcropthanthetreesinunloggedforestevenafteraccountingfortreesizeandthefunctionalroleofvertebratesinseedpredationincreasedinloggedforestwhilethatof non-vertebrates declined The strength of density-dependencein dipterocarpsmay change frompositive to negative at differentlife stages (Blundell amp Peart 2004 Curran ampWebb 2000) Thisappearedtobethecase inunloggedforestwheregermination in-creasedwithlocal-scaleconspecificseeddensitypossiblybecausepredatorsweresatiatedbythehighmast-fruitingseeddensitiesbutseedlingsurvivaltendedtodecline(Figure5afTable1bc)HoweverinconsistentwithourpredictionofstrongerNDDinloggedforestgermination and especially seedling survival increasedwith local-scaleconspecificseeddensitywhichsuggeststhatloggingmayhaveaffectedpredator-mediatedNDDduringtheseed-to-seedlingtran-sitionbottleneck inD lanceolata Importantlyourfindingsappliedtoamast-fruitingyearwhenmostdipterocarprecruitmentoccurs(CurranampLeighton2000Janzen1974)suggestingthat intensiveloggingmaypotentiallyaffectlong-termpopulationdynamicsofD lanceolataOur findings add to knowledge of how ecological pro-cesses responsible for themaintenanceofbiodiversitymaybeaf-fectedbylogging(DarrigodosSantosampVenticinque2018Ewersetal2015Schleuningetal2011Woodcocketal2013)
Increasing edaphic and drought stress in reproducing treesin logged forest may have contributed to the reduced seed crop(Curran etal 1999 Hardwick etal 2015) The consequences ofseed limitation in logged forests for sapling and ultimately adulttree recruitment remain largelyunexploredbutmaybedetrimen-tal for long-term tree population dynamics (Caughlin etal 2015)Changes in the functional roles of non-vertebrate seed predators
8238emsp |emsp emspensp PILLAY et AL
relativetovertebratesinloggedforestmaybedrivenbynumericalchanges inpredatorabundanceacrossgroups (Ewersetal2015)The altered microclimatic conditions in logged forests are likelyhostile to populations of insect seed predators and fungal patho-gens(Ewersetal2015Hardwicketal2015)Converselylogged
forestsmayprovideincreasedresourceavailabilityforrodentseedpredatorsandthusbenefittheirpopulations(Ewersetal2015)
Theuniqueecologyofmast-fruitingandtheimpactthisphenom-enonmayhavesustainedinloggedforestmayexplainthecomplexdensity-dependent patterns of germination and seedling survival(Figure5af)On theonehand in unlogged forest predator satia-tionmayhavebeenoccurringatthehighseeddensitiesduringthemast(Janzen1970)aspotentiallysupportedbyourfindingthatger-minationtendedtoincreasewithhigherseedfall(Figure5cBagchietal2011CurranampWebb2000)Indeedmast-fruitinghasbeenhypothesizedtobeanevolutionaryresponsetodensity-dependentmortality factors allowing seeds to escape predation by satiatingseedpredators (Janzen19701974)Ontheotherhand in loggedforesttheconcentratedseeddensitiesunderspatiallyisolatedadulttreesmayallowNDDtooperate(Bagchietal2011CurranampWebb2000)Howeverourfindingsofincreasedgerminationandespeciallyseedlingsurvivalwithhigherconspecificseeddensityinloggedfor-est(Figure5afTable1bc)werecontrarytotheexpectationsunderNDDandmaybeassociatedwiththediminishedfunctionalroleofnon-vertebrate seedpredators in logged forest (Figure4)NDD isprimarily driven by host-specific insect seed predators and fungalpathogenswhichtendtoconcentrateamongthehigh-seedseedingdensitiesunderthecrownsofparenttreestherebycausinghighermortalitywhere densities are higher (Bagchi etal 2014 Connell1971 Janzen 1970) These non-vertebrate seed predators andpathogensmaybedeclining in logged forests (Ewers etal 2015)andtheirecologicalroleinmaintainingNDDmaybediminishedIncontrastthetendencyofvertebratestoforageoverlargeareasmayrender predation-relatedmortality to bemore spatially heteroge-neousrelativetoseedseedlingdensities(SwamyampTerborgh2010)
Wenotethatseedcropsizegerminationandseedlingsurvivaltendedtoincreaseforlargertreesinbothforesttypes(Figures3c5di)Thissuggeststhatselectiveloggingpracticesthatharvesttim-ber at sustainable rates and followsilviculturalpracticesdesignedtominimizedamagetotheresidualstand(Asneretal2009Martinetal2015Putzetal2012)arecriticaltopreventseedlingrecruit-mentfailure indipterocarpforestsSeedgerminationandseedlingsurvivalofD lanceolatatendstobepositivelyassociatedwithlightavailability (Itoh etal 1995) which likely explains why seed andseedling mortality tended to increase with higher canopy cover(Figure5ej)
41emsp|emspCaveats and limitations
OurstudyincludedsevenandsixD lanceolatatreesasindepend-ent experimental units in unlogged and logged forests respec-tively (cfBagchietal2011HolbrookampLoiselle2009Poulsenetal 2012) The spatially clumped distributions of most adultfruiting individuals inunlogged forestand the fewspatially scat-teredadultdipterocarpsremaininginloggedforest(ofallspeciesD lanceolata was the most abundant at seven individuals) pre-cludedadditionalreplicationatthelevelofindividualtreeswithinforesttypeThesparsenumberofadultdipterocarpsinthelogged
TABLE 1emspModelaveragedestimatesexplainingvariationin(a)seedcropsize(b)germinationand(c)seedlingsurvival(upto3monthsafterseedfall)ofD lanceolatainrelationtothepredictorvariablesthatweresupportedbyAICc-basedmodelselectioncriteria(SupportinginformationTablesS2S6S7)
Response and predictor variables Estimate (SE) 95 CI
(a)Seedcropsize
Intercept 300(029) 240ndash352
Loggedforest minus080(048) minus172ndash007
Distance minus013 (001) minus014tominus011
Loggedforesttimesdistance minus001(001) minus005ndash001
Treesize 006(014) minus018ndash060
Loggedforesttimestreesize 001(010) minus054ndash080
(b)Germination
Logged forest 468 (362) 269ndash1096
Conspecific seed density minus271 (238) minus744tominus075
Logged foresttimesconspecific seed density
265 (235) 105ndash723
Distance 003(018) minus062ndash133
Loggedforesttimesdistance minus002(016) minus134ndash091
Seedfall minus084(157) minus602ndash104
Loggedforesttimesseedfall 024(149) minus422ndash1428
Treesize minus018(098) minus639ndash329
Loggedforesttimestreesize minus014(108) minus1072ndash474
Canopycover 001(032) minus217ndash255
Loggedforesttimescanopycover 015(084) minus155ndash775
(c)Seedlingsurvival
Loggedforest minus710(403) minus1500ndash081
Conspecificseedlingdensity 030(015) minus001ndash060
Logged foresttimesconspecific seedling density
minus170 (043) minus255tominus086
Distance 015 (009) 002ndash032
Logged foresttimesdistance minus104 (067) minus231 tominus012
Seedfall 003(058) minus119ndash126
Loggedforesttimesseedfall minus203(307) minus863ndash389
Treesize minus003(096) minus206ndash199
Logged foresttimestree size minus316 (205) minus706 tominus033
Canopycover 027(028) minus024ndash087
Loggedforesttimescanopycover minus034(110) minus271to191
NotesResultsforseedcropsizerepresentcoefficients(log-scale)esti-matedwithgeneralizedlinearmixedmodelsResultsforgerminationandseedling survival represent loghazardsestimatedwithCox regressionmixed-effectssurvivalmodelsEstimatesinitalicsindicatethatthe95confidenceintervalsdidnotoverlapzerosuggestingastrongeffectofthepredictorvariableonthecorrespondingresponsevariable
emspensp emsp | emsp8239PILLAY et AL
forestisareflectionofthepopulationreductionmanytimbertreespeciesaresubjected toafter intensiveselective logging (Martinetal2015)
The variable density of adultD lanceolata trees between un-logged and logged forests may introduce confounding negativedensity-dependentneighbourhoodeffectsonseedlingrecruitment(BlundellampPeart2004StollampNewbery2005)PreviousresearchontheDipterocarpaceaesuggeststhatneighbourhoodeffectsmayoccurwhenconspecificadultsarewithin20mofeachother(StollampNewbery2005)Ourrequirementofnon-overlappingseedshad-owsbetweenfocaltreesensuredthattreeswereseparatedbyatleast40mTherelativelylargerdistancebetweenthefocaltreesinourstudycomparedwiththethresholddistanceof20matwhichneighbourhoodeffectsmayoccur(StollampNewbery2005)shouldthusservetominimizethispotentialconfoundingfactor
Inanalyzingagentsofseedandseedlingpredationwedidnotdistinguishbetweenthedifferentprocessesofseedlingpredation
andherbivoryOftheseedlingsthatwerealiveinthenaturalplotsat the end of the study 017 and 176 showed signs of leafdamagetypicalofinsectherbivory(ColeyampBarone1996)inun-loggedandloggedforestsrespectively Intheexperimentalandpairedcontrolplotsthepercentageofseedlingswithsignsofleafdamage fromherbivorywas similarly small (061and065 inunloggedand logged forest respectively)Thusobservedseed-lingherbivoryrateswerelowAlonger-termstudymayrevealal-teredseedlingherbivoryrateswithlogging(Darrigoetal2018)particularly because herbivorous insect biomass was found toincrease with logging (Ewers etal 2015) Our study examinestheeffectsofintensiveselectiveloggingontheseed-to-seedlingtransitionphaseofacanopydipterocarpHoweverour findingsmaynot represent the fateofseedlingsovera longer timespanbecause ecological changes caused by logging (eg herbivory)could continue to impact the survival of seedlings beyond theseed-to-seedlingtransitionbottleneck(Caughlinetal2015)
F IGURE 4emspTheoddsofpredationofD lanceolataseedsbyvertebratesrelativetonon-vertebratesin(a)naturalplotsand(b)experimental(vertebrateexclosures)andpairedcontrolplotsinunloggedandloggedforestErrorbarsrepresent95confidenceintervals
(a) (b)
F IGURE 5emspTherelationshipsbetweenD lanceolataseedgermination(toppanel)seedlingsurvival(bottompanel)and(af)conspecificseedseedlingdensity(bg)distancefromtheparenttree(ch)seedfall(di)treesizeand(ej)canopycoverinunloggedandloggedforests
(a) (b) (c) (d) (e)
(f) (g) (h) (i) (j)
8240emsp |emsp emspensp PILLAY et AL
WedidnotmanipulatedensityanddistanceindependentlyOuruseof seeddensity gradientsnaturally generatedby thedistancegradient can identify density-dependent patterns of seedling re-cruitment (Harms etal 2000Webbamp Peart 1999)However intheabsenceofexperimentalmanipulationofdensityanddistanceeffects independent of each other our ability to understand thecauses underlying observed patterns of density-dependence inunloggedand logged forests is limited (SwamyampTerborgh2010)Futurestudiesshouldleveragemanipulativeexperimentsforanu-ancedunderstandingof the causes underlying alteredpatterns ofseedling recruitment in the face of anthropogenic disturbances(FreckletonampLewis2006)
5emsp |emspCONCLUSION
We found that for Dryobalanops lanceolata a dipterocarp spe-ciesendangeredby thecommercial timber trade (Ashton1998)multiple stages of seedling recruitment were altered in selec-tively logged forest compared with unlogged forest during amast-fruiting year Future studies should leverage broader log-ging gradients additional species and experimental approachesover longer time frames (Bagchietal2011Martinetal2015Riuttaetal2018Struebigetal2013SwamyampTerborgh2010)to quantify the thresholds of logging intensity abovewhich theecologicalprocessofseedlingrecruitmentmayunravelWehigh-lighttheimportanceofunderstandingtheimpactsofdisturbancessuch as logging on ecological processeswhich can complementnumericalassessmentsofbiodiversitytounmaskimpactsthatmayotherwiseremainhidden
ACKNOWLEDG MENTS
We thank Yayasan Sabah BentaWawasan Sdn Bhd the SabahBiodiversity Council the Sabah Forestry Department theMaliauBasin Management Committee the State Secretary Sabah ChiefMinisterrsquosDepartmenttheMalaysianEconomicPlanningUnitandtheRoyalSocietySouthEastAsiaRainforestResearchPartnershipfor granting permits Our fieldwork was funded by grants fromthe Rufford Small Grants Foundation IDEAWild the Institute ofFoodandAgriculturalSciencesandtheTropicalConservationandDevelopmentProgramattheUniversityofFloridaWethankRyanGray andMinSheng Khoo for coordinating field logistics MainusTausong JeffryAminMohdYusufDidin (Roy)RismanAjangandMelvin Teronggoh for assistance during fieldwork Magat JaparandJeffryAminfor identifyingtreesseedsandseedlingsJeffreyHostetler forhelpwith survival analysis andEmilioBrunaTrevorCaughlin David Newbery and one anonymous reviewer for con-structivecommentsthatgreatlyimprovedthemanuscript
CONFLIC T OF INTERE S T
Nonedeclared
AUTHOR CONTRIBUTIONS
RPconceivedthisstudyRPandRJFraisedthegrantsforfieldworkRPBALRJFandHBdesignedthemethodologyRPcollectedthedataandperformedallstatisticalanalysesRPandFHledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandprovidedfinalapprovalforpublication
DATA ACCE SSIBILIT Y
DatacanbeaccessedthroughtheDryadDigitalRepositoryhttpsdoiorg105061dryaddk4t694 (Pillay Hua Loiselle Bernard ampFletcher2018)
ORCID
Rajeev Pillay httporcidorg0000-0002-7116-6855
R E FE R E N C E S
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BagchiRGalleryREGripenbergSGurrSJNarayanLAddisCEhellipLewisOT(2014)Pathogensandinsectherbivoresdriverain-forestplantdiversityandcompositionNature50685ndash88httpsdoiorg101038nature12911
Bagchi R Philipson C D Slade E M Hector A Phillips SVillanueva J F hellip Press M C (2011) Impacts of logging ondensity-dependentpredationofdipterocarpseedsinaSouthEastAsian rainforestPhilosophical Transactions of the Royal Society B Biological Sciences 366 3246ndash3255 httpsdoiorg101098rstb20110034
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BornJBagchiRBurslemDNilusRTellenbachCPluessARampGhazoulJ(2015)DifferentialresponsesofdipterocarpseedlingstosoilmoistureandmicrotopographyBiotropica4749ndash58httpsdoiorg101111btp12180
BrunaEM (1999) Seedgermination in rainforest fragmentsNature402139httpsdoiorg10103845963
BurnhamKPampAndersonDR(2002)Model Selection and Multimodel Inference A Practical Information-Theoretic ApproachNewYorkNYSpringer-Verlaghttpsdoiorg101007b97636
Caughlin T T Ferguson J M Lichstein J W Zuidema P ABunyavejchewinSampLeveyD J (2015)Lossofanimal seeddis-persalincreasesextinctionriskinatropicaltreespeciesduetoper-vasivenegativedensitydependenceacross life stagesProceedings of the Royal Society B Biological Sciences28220142095httpsdoiorg101098rspb20142095
ChambersJCampMacMahonJA (1994)Adayinthe lifeofaseedMovementsandfatesofseedsandtheirimplicationsfornaturaland
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managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
8232emsp |emsp emspensp PILLAY et AL
1emsp |emspINTRODUC TION
Vastareasofnatural forestarebeingdegradedaroundtheworldInthetropicsselectiveloggingcharacterizedbyunsustainablehar-vest rates and improper silvicultural practices is amajor driver offorestdegradation (AsnerRudelAideDefriesampEmerson2009MartinNewtonPfeiferKhooampBullock2015Putzetal2012)Theconsensusofrecentinsightsintohowselectivelogging(hereaf-terldquologgingrdquo)affectsbiodiversityisthatmostspeciesacrosstaxo-nomicgroupsappeartopersistinloggedforests(EdwardsTobiasSheilMeijaardampLaurance2014Putzetal2012WilcoveGiamEdwards Fisher amp Koh 2013)What remains poorly understoodhoweverishowloggingmayaffectnumerousecologicalprocessesthatarethefoundationofecosystemfunctioningandmaintenance(Ewersetal2015Schleuningetal2011)Seedlingrecruitmentisamongthefundamentalprocessesthatdeterminethemaintenanceofplantdiversityinforestecosystems(Wright2002)andisade-mographic bottleneck in plant population dynamics (Chambers ampMacMahon1994Chesson2000PoulsenClarkampBolker2012)In theaftermathofdisturbances suchas logging seedling recruit-mentofcanopytrees isvital for forest regenerationandrecovery(Bagchi etal 2011 Chazdon 2003) Despite its importance ourknowledgeoftheimpactofloggingonseedlingrecruitmentislim-ited(Bagchietal2011Curranetal1999)
There are several pathways by which logging may impactseedling recruitment First the removal of the largest andmostreproductively active trees (Fisher etal 2011) may directly re-ducetotalseedproductionatthescaleofthe landscape (Bagchietal 2011)The remaining treesmayalsobecomespatially iso-lated from reproductive conspecifics which may reduce cross-pollinationandindirectlydecreaseseedcropsizeatthescaleofindividualtrees(GhazoulListonampBoyle1998MurawskiNimalGunatillekeampBawa1994)Secondthespatial isolationofadulttrees from conspecifics in logged forestsmay concentrate seedpredatorsatthesetrees(Bagchietal2011)potentiallyincreasingthe strengthofpredator-mediatednegativedensity-dependence(NDD)aprocessthatunderliesseedlingrecruitmentbeyondtheseed production stage (Bagchi etal 2014 Swamy amp Terborgh2010)NDD or the tendency for seeds and seedlings to exhibitreducedsurvivalwithincreasedconspecificdensityatlocalscalesisapervasivedemographicforcethatmaintainsplantcommunitydiversitybypreventingthedominanceofcommonspecies(Bagchietal 2014 Comita Muller-Landau Aguilar amp Hubbell 2010Connell 1971 Harms Wright Calderoacuten Hernaacutendez amp Herre2000 Janzen 1970WebbampPeart 1999) Third seedpredatorcommunities comprising insects fungal pathogens and verte-brates may undergo population shifts in logged forests (Ewersetal 2015) The functional roles playedby various seedpreda-torsmayalsochange(Ewersetal2015)potentiallyalteringthestrengthofNDDinconstrainingtherecruitmentofcommonspe-cies (Bagchietal2011)Fourthseeds in loggedforestsmaybeexposed to increased light penetration and hotter drier air andsoilconditionsduetotherelativelyopencanopy(Hardwicketal
2015)Theseabioticfactorscannegativelyaffectseedlingrecruit-ment(Bruna1999)Thusmultiplestagesofseedlingrecruitmentmaybealteredinforestsdegradedbylogging
Understandinghowloggingmayimpactvariousstagesofseed-lingrecruitmentisaparticularlyrelevantissueinthedipterocarp-dominated (Family Dipterocarpaceae) tropical rainforests ofSoutheastAsiaNot only is this ecosystem imperiled by logging(Asner etal 2009) but its unique mast-fruiting ecology alsolikelyrenders itsseedlingrecruitmentprocesstoresponddiffer-ently to loggingcomparedwithother tropical forestecosystems(Bagchietal2011)Mast-fruiting inSoutheastAsianrainforestsoccursapproximatelyevery3ndash9years (Janzen1974)andistypi-callycommunitywideupto88ofcanopytreespeciesmayfruitsynchronously (Curran amp Leighton 2000 Curran etal 1999)For dipterocarps many species of which are targets of logging(SoepadmoSawampChung2002SoepadmoampWong1995)mast-fruiting years account for the majority of seedling recruitment(CurranampLeighton2000Janzen1974)Impactsondipterocarpseedling recruitment during mast-fruiting years may thereforehavedisproportionatelyimportantconsequencesfortherecoveryofloggedforestsinSoutheastAsia(Bagchietal2011CurranampLeighton2000)WhileitisknownthatdipterocarpsmayundergorecruitmentfailureinloggedforestsofSoutheastAsiaduringnon-mast years (Bagchi etal 2011) empirical understandingofhowvarious stages of seedling recruitment are impacted by loggingduring mast-fruiting years is limited (Curran amp Leighton 2000CurranampWebb2000)
Herewe investigate the impactof loggingon theseedling re-cruitment process of an endemic and endangered dipterocarpspeciesheavily targetedby loggingDryobalanops lanceolataBurck(Ashton 1998) during a mast-fruiting event in Sabah BorneoWe combined natural observations and an exclosure experimentoveronemast-fruitingseasontotestthefollowingpredictions (1)Loggingremovesthe largestmostreproductivelyactivetreesandmayincreasethespatialisolationoftheremainingtreesrelativetoeachotherThereforeweexpectedtheseedcropwouldbesmallerin logged forest than in unlogged forest (2) Vertebrate and non-vertebrate seed predator communities in logged forests may un-dergopopulationincreasesanddeclinesrespectively(Ewersetal2015)Consequentlyweexpectedthefunctionalroleofvertebratesin seed predation to increase and that of non-vertebrates to de-creaseinloggedforest(3)Althoughthehighseeddensitiestypicalof SoutheastAsianmast-fruiting forests usually reduce seedmor-talitybysatiatingpredators(Janzen19701974)wepredictedtheconcentratedseeddensitiesunderspatiallyisolatedtreesinloggedforestsmayallowNDDtooperate(Bagchietal2011)Thereforewe expected the relationship between seedling recruitment andlocal-scale conspecific seed density would be stronger in loggedforestthaninunloggedforestWefocusedontheseed-to-seedlingtransitionphaseover3monthsafterseedfallademographicbottle-neckthatdisproportionatelyinfluencesthestructuredynamicsandcomposition of tree communities (Chambers ampMacMahon 1994Chesson2000Poulsenetal2012)
emspensp emsp | emsp8233PILLAY et AL
2emsp |emspMATERIAL S AND METHODS
21emsp|emspStudy area
Weconductedfieldworkintwodipterocarp-dominatedforestsitesspaced 65km apart in Sabah Malaysian Borneo These sites arepart of the experimental design of the Stability of Altered ForestEcosystems(SAFE)Project(Ewersetal2011)andencompasspri-maryforestwithintheMaliauBasinConservationArea(MBCA)andrepeatedlyloggedforestwithintheKalabakanForestReserve(KFR)aloggingconcessionintheYayasanSabahForestManagementAreaOverallthelogginggradientencompassedwithintheSAFEexperi-mental design resembles the pattern of habitat conversion acrossthewiderregion(Ewersetal2011Struebigetal2013)
TheforestatMBCA(a5884km2protectedarea)representsthenearest topographicallymatchedprimary forest to the logged for-est inKFR(Ewersetal2011Struebigetal2013)Thetwositesarealsosimilar intermsofsoilnutrientprofilesandphysicalprop-erties(Riuttaetal2018)TheMBCAservesastheunloggedcon-trolsiteof theSAFEProject (Ewersetal2011)Twoof thethreecontrolblocks atMBCA (hereafter ldquounlogged forestrdquo) (OG1OG2)haveneverbeenloggedwhilethethird(OG3)waslightlyloggedinthe1970sand1990s (seeEwersetal2011)AspartoftheSAFEProjectexperimentalforestfragments(110100ha)arebeingcre-atedinKFR(Ewersetal2011)PriortothisexperimentKFRwassubjectedtomultiplerotationsofloggingthefirstofwhichbeganinthe1970s(Chong2005Fisheretal2011)Commerciallyvalu-abletreesgt60cmdiameteratbreastheight(DBH)wereextractedand11296m3haoftimberwasremoved(Fisheretal2011)Thesecond rotation commencing in the 2000s (Chong 2005 Fisheretal2011)encompassedthreeroundsduringwhichtreesgt40cmDBH were targeted (Fisher etal 2011 Struebig etal 2013) Avolumeof25872232 and1816m3haof timberwasextractedduringeachroundrespectively(YayasanSabahunpublisheddata)Logging ended in 2007ndash2008 (Fisher etal 2011) by which time17931m3haof timberwascumulatively removed (Struebigetal
2013)Extensivecollateraldamagetoforeststructurealsooccurredduetotheestablishmentofskidtrailsaccessroadsandlog-landingareas (WearnRowcliffeCarboneBernardampEwers2013)Thustheloggingintensitywasaround45timesthethresholdoflt40m3habeyondwhichresidualstanddamagesurpassesthe25ndash30limitconsidered sustainable (Martin etal 2015) The six experimentalblocks(AndashF)atSAFE(hereafterldquologgedforestrdquo)(Ewersetal2011)comprise a heterogeneous landscape that has been subjected tovaryingintensitiesandtimingsoftimberextraction
22emsp|emspStudy species
Dryobalanops lanceolataBurckisanemergenttreethatcangrowupto80mhigh(Soepadmoetal2002)EndemictoBorneoitiswide-spread and common in the statesof Sabah andSarawak growinginmixed-dipterocarp forestonclay-richsoils (SoepadmoampWong1995Soepadmoetal2002)Thesaplingsareshadetolerant(ItohYamakuraOginoampLee1995)andcansurvivemanyyearsexpand-inghorizontallyuntilacanopygapopensup(Soepadmoetal2002)It is ahardwoodspeciesvalued for its construction timber that issoldunder the tradenameKapur (Soepadmoetal 2002)Due tocommercialharvestingandhabitat loss it isnowrareoutsidepro-tectedareasand isclassifiedasEndangered(IUCNRedListv23Ashton 1998) Like other dipterocarps its winged seeds are dis-persedbygyration (Figure1)andmostly fall incloseproximity tothecrownoftheparenttree(ItohYamakuraOginoLeeampAshton1997)Itsseedsandseedlingsareattackedbyfungalpathogens(per-sonal observation)insectsandvertebratessuchasbeardedpigs(Sus barbatus)andvariousspeciesofrodents(Itohetal1995)
23emsp|emspStudy design
Weconductedfieldworkduringamast-fruitingeventthatoccurredin2014 InJuneandJulyprior to thecommencementofseedfallwe surveyed ~2146km of forest trails that passed through thediametersof the110 and100ha ldquofragmentsrdquoofBlocksABD
F IGURE 1emspDryobalanops lanceolataisanendangereddipterocarpendemictoBorneoTheseedsarewinddispersedandmostlyfallneartheparenttreeLeftAmatureseedgerminatingD lanceolataseedshavefivewingsandaregreenwhentheyfallfromthetreebutturnpinkupongerminationwithin5ndash7daysofdispersalCenterMarkedseedlingsinanaturalplotRightSeedlingsinanexperimental(vertebrateexclosure)plotPhotocreditsRajeevPillay
8234emsp |emsp emspensp PILLAY et AL
E andF in the logged forest andwere able to locate only sevenadultD lanceolatatreesinactivefruitingcondition(withinBlockEtwotreeswithinandaroundBlockFfivetrees)OneofthetreesinBlockEwaslt40mfromtheotherreproductiveconspecificWeremovedthis individual fromthisstudytoensurenon-overlappingseedshadowssincepriorworkonD lanceolatainSarawakBorneo(Itohetal1997)indicatesthatallseedsaredispersedlt40mfromthe parent treeWe included the remaining six individuals in thisstudyThusthesparsenumberofadultconspecificsinactivefruit-ingconditiondictatedoursamplesizeatthelevelofindividualtreesIn the unlogged forest sitewe surveyed approximately 65kmofforesttrailseachinBlocksOG1andOG2andlocated15ndash20(OG1)and20ndash25(OG2)adultD lanceolatatreesinactivefruitingcondition(weexcludedOG3fromthisstudydueto its logginghistory)TheseedshadowsofalltreesinOG1overlappedwiththoseofatleastoneotherconspecificadultThereforeweselectedsevenindividu-alsinOG2whoseseedshadowsdidnotoverlapwiththoseofotherreproductiveconspecificsWeconsideredeachindividualfocaltreeasanexperimentalunitresultinginsevenandsixreplicatesatthelevelofindividualtreesinunloggedandloggedforestrespectivelyIndividualtreesareoftenusedasexperimentalunitsinseeddisper-salandseedlingrecruitmentstudiesandmaybeconsidered inde-pendentsamplesiftheirseedshadowsdonotoverlapwiththoseofotherconspecifics (Bagchietal2011HolbrookampLoiselle2009Poulsenetal2012)
Thesevenfocaltreesinunloggedforestwere303mapartonaveragewith the smallest pairwise distance between two treesbeing40mThesixfocaltreesinloggedforestwere1690mapartonaveragewiththesmallestpairwisedistancebetweentwotreesbeing244mandcoverconsiderable landscapeheterogeneity interms of logging intensity and time since logging (Wearn etal2013)Onaverageourfocaltreeswerearound56timesfurtherapart from each other in logged forest than in unlogged forestwhichpotentiallyindicatestheintensityofextractionifD lance-olatapopulationdensitiesweresimilar inbothforesttypespriortologging
Wesetupfour32mtransectsextendingfromthebaseofeachfocaltreewiththefirsttransectorientedalongarandomcompassdirection and each subsequent transect at 90deg from the previous(Figure2)We constrained transect length to 32m because priorwork indicated that few seeds reached this distance (Itoh etal1997)AlongeachtransectweusedseedtrapstoquantifytheseedcropandseeddispersaldistancesettingthemupsoonafterseedfallcommencedinearlyAugust2014Wedeployedtheseedtrapsonalog2scaleat124816and32mdistances(n=24seedtrapstreeFigure2)Eachtrapwasa1times1mnylonmeshnetsuspendedby1-mtallPVCpipesateachcornerThevalidityofourdatareliesontheassumptionthatourfocaltreeshadnon-overlappingseedshadowsSince995of all seeds fell into the seed trapswithin16m fromtheirrespectiveparenttrees(seeSection3)adistancethat is lessthanhalfoftheminimumdistancebetweenanyofourfocal trees(ie40m)theseedsweincludedinthisstudyshouldbepredomi-nantlyifnotentirelyfromtheirrespectiveparenttrees
Wemonitoredseedpredationanddensity-dependentpatternsofgerminationandseedlingsurvivalof individualseedsthatnatu-rally dispersed into individual 1times1m unmanipulated monitoringplots (hereafter ldquonatural plotsrdquo) We thus utilized the conspecificseedseedlingdensitygradientnaturallygeneratedbythedistancegradient forourassessmentofNDDWeplacednaturalplots2mtotheleftoftheseedtrapsalongeachtransectat24816and32m distances (n=20 natural plotstree Figure2) Additionallyaround 1month after the commencement of seedfall we set upvertebrate-exclosure plots (hereafter ldquoexperimental plotsrdquo) andpairednon-exclosureplots(hereafterldquocontrolplotsrdquo)totestfortherelativecontributionofvertebratesversusinsectsandfungitoseedpredationWeplacedexperimentalandcontrolplotsat2and32mdistancesalongone randomlyselected transectateach focal tree(n=2 plot pairstree Figure2)At 32mweplaced eachplot pair2mfromeachotherandontherightsideofthecorrespondingseedtraprandomlyassigningtherelativepositionofexperimentalversuscontrolplots(iewhichplotwasplacedadjacenttothecorrespond-ingseedtrap)At2mduetolimitedspacenearthebaseofthefocaltreeweplacedoneplotontherightofthecorrespondingseedtrapandthepairedplotatthecorrespondingpositionalongthediago-nallyoppositetransectrandomlyassigningtherelativepositionofexperimentalversuscontrolplots (Figure2)Dueto logisticalcon-straintsweomittedoneof themost remote focal trees in loggedforestinthiscomparisonandinsteadsetuptwoadditionalplotpairsinthesamewayaroundanotherofourfocaltreeswhichwasmore
F IGURE 2emspStudydesignshowingseedtraps(at124816and32mdistances)naturalplots(at24816and32mdistances)andpairedexperimental(vertebrateexclosures)andcontrolplots(at2and32mdistances)alongfour-32mtransectsfromthebaseoffocalD lanceolatatreesSeedtrapsnaturalandcontrolplotswere1times1minareaExperimentalplotswere1times1times05mFigurenottoscale
12 4 8 16 32
Focal treeSeed trapNatural plotExperimental plotControl plot
emspensp emsp | emsp8235PILLAY et AL
accessible Experimental plotswere 1times1times05mwith the exclo-suremade fromsteelwireof127times127cmmeshsize toexcludeallvertebrateseedpredatorsbutnotinsectseedpredatorsorfungalpathogens(Figure1)Controlplotswereopentoallseedpredatorsandpathogens
ForthepairedexperimentalandcontrolplotsweaddedD lance-olataseedsatpredefineddensities~1monthaftercommencementof seedfall and thereafter continuously removed all conspecificseedsthatfellintothecontrolplotsthroughoutthedurationofthestudyWeused a seeddensity of 5seedsm2 for thepairedplotsat2mdistancesand50seedsm2 forthoseat32mdistancesForseeding the plots we collected intact (ie no visible evidence ofpredatorattack)matureseedsfromaround20non-focalD lanceo-latatreesinunloggedforestWethoroughlymixedtheseseedsandplacedthemonthesoilsurfaceinaregulargridtomimicthenaturalseedfallpatterninwhichseedsgyratefromtheparenttreesandlandonthegroundWethusdistributed770seeds(n=28experimentalandpairedcontrolplots)ineachforesttypeWenotethatthispartofthestudyaimstoprovideonlyasupportingassessmentoftherel-ative importanceofvertebrateandnon-vertebrateseedpredatorsinunloggedandloggedforestsWedidnotattempttomanipulatedensity anddistance independentlydue to logisticaldifficulties incollecting and sowing additional seeds a time-sensitive undertak-ingbecauseoftherapidityatwhichseedsgerminatetogenerateaspectrumofseeddensities thatwouldreflectscenariosunderun-loggedandloggedconditions(cfBagchietal2011Poulsenetal2012)
24emsp|emspData collection
We collected seeds from the traps at two census intervals be-tween12Augustand4Novemberinloggedforestandbetween1Septemberand22October inunloggedforestWemonitoredthefateofeveryseeduponinitiatingthenaturalplots(atthesameinter-valsastheseedtraps)untiltheendofthestudyWetaggedallseedswithnumberedplastictagsstapledtotheirwings(Figure1)andcon-tinuedtaggingseedsthatnewlyfell intothenaturalplotsAteachcensusintervalwerecordedthenumberofseedsthatsurvivedanddiedineachplotForsurvivingseedswerecordediftheywereger-minatingandsubsequentlywhether they recruited into seedlingsWealsoscoredeachseedintooneofthefollowingcategories(afterBagchietal2011)intact(novisiblesignsoffungalinsectorverte-brateattack)germinated(definedasemergenceoftheradicleItohetal1995)seedling(ge5cmtallexpandedtrueleaves)vertebratedepredated(partiallyeatengnawedorremoved)insectdepredated(withentryexitholes) fungusdepredated(withfungalsporesmy-celia)Wenote that the seeds falling into the natural plotswouldlikely be exposed to both pre-dispersal and postdispersal insectpredators(Bagchietal2011)Wewerecarefultoclassifydepreda-tionstatusonthebasisofthepredatorthatweinitiallyrecordedtohaveattackedtheseedseedling(LewisampGripenberg2008)Thusaseedwithinsectentryexitholesattheinitialcensusthatwassub-sequentlypartiallyeatenorremovedbyvertebrateswasscoredas
predatedbyinsectsDuetothedifficultyinascertainingtheinitialpredatorbetweeninsectsandfungalpathogenswecollapsedthemintothenon-vertebratecategoryWethususedtwopredatorcat-egoriesvertebrateversusnon-vertebrate
WemeasuredasetofecologicalcovariatesthatcanpotentiallyinfluencevariousstagesofseedlingrecruitmentandthusshouldbeaccountedforinexaminingtheimpactsofloggingThesecovariatesincludedthreemeasuresoftreesizethataredeterminantsofseedcropsizeanddispersaldistanceDBHheightandcrowndiameter(CousensDythamampLaw2008NorghauerNockampGrogan2011)We also measured percentage canopy cover as a proxy for lightavailabilitywhich in turnmay influencegerminationand seedlingsurvival(Kobe1999)SeeSupportinginformationAppendixS1fordetailsonthesemeasurements
25emsp|emspStatistical analyses
Wefirstusedprincipal-componentsanalysis(PCA)toidentifymajortrends intreesizedataandreducethenumberofvariablesrepre-sentingtreesizeThefirstprincipalcomponent(PC1)waspositivelycorrelatedwithallthreevariablesrepresentingtreesizehadanei-genvaluegt1andexplained764ofthetotalvarianceintreesizedata (Supporting information Table S1) We used the componentscoresgeneratedfromthe loadingsofPC1asasurrogatefor treesizeinfurtherstatisticalanalyses
Wethenusedgeneralizedlinearmixedmodels(GLMMs)toana-lyzetheimpactsofloggingonseedcropsizeanddispersalpatternsusingthenumberofseeds ineachseedtrapastheresponsevari-ableWeusedforesttype(unloggedvslogged)distancefromthefocaltreePC1(hereafterldquotreesizerdquo)andalltwo-wayinteractionsbetween forest type and the other variables as fixed effectsWeincluded individualseedtrapsnestedwithintreesasa random in-terceptinallmodelsWeassumedaPoissonerrordistributionandaloglinkfunctionWetestedforoverdispersionbycalculatingthesumofsquaredPearsonresidualsandcomparing it totheresidualdegreesoffreedomforeachmodel(ZuurIenoWalkerSavelievampSmith2009)
WealsousedGLMMstoanalyzetheimpactofloggingontherelative role of vertebrates versus non-vertebrates inD lanceo-lataseedandseedlingpredationOurobservationsindicatedthatmostseedlingsdiedfrompredation(eguprootedandpartiallycompletelyconsumedremovedbyvertebratescotyledonsofger-minatedseedlingsdestroyedbyinsectsandorfungalpathogens)rather than from leaf damage typically inflicted by herbivores(ColeyampBarone1996)Thereforewepooleddataon seedandseedling predation For the natural plotswe scored each seedseedling as depredated by either vertebrate or non-vertebratepredators and then modeled the probability of a seedseedlingbeingdepredatedbyvertebrates (relative tonon-vertebrates)asa functionof forest typeas the fixedeffectvariableForpairedexperimental and controlplotswecounted thenumberofdep-redated seedsseedlings out of the total number of seeds andthenmodeledtheprobabilityofseedseedlingpredationWeused
8236emsp |emsp emspensp PILLAY et AL
foresttypeandtreatmenttype(experimentalvscontrolplots)asfixedeffectvariablesInbothanalysesofseedseedlingpredationweincludedindividualplotssequentiallynestedwithintransectsandtreesasarandominterceptWeassumedabinomialerrordis-tribution and a logit link functionWe note that nomadic herdsof bearded pigs destroyed our experimental exclosures for fourout of seven trees in unlogged forest (but not in logged forest)between1and19October(~30daysfromtheonsetofseedseed-lingmonitoringintheseplots)Thereforeforunloggedforestweonly considered data from the paired experimental and controlplotsforthethreetreesthatwerenotdepredatedbybeardedpigs(n=330seeds12plots)
WeusedCoxregressionmixed-effectssurvivalmodelstoan-alyzethe impactof loggingongerminationandseedlingsurvivalatthelevelofindividualseedsandseedlingswithdatacollectedfromthenaturalplotsWefirstmodeledseedsurvivaluntilger-minationwithsurvivalmodeledasdailygerminationrateOftheseeds that germinatedwe subsequentlymodeled daily seedlingsurvivaluntil3monthsafterseedfallWeincorporatedseedseed-lingageandusedright-censoring ifaseedseedlingsurvivedbe-yondtheendofthemonitoringperiodForfixedeffectvariablesweincludedforesttypelocal-scale(1m2)conspecificseedseed-lingdensity (hereafter ldquoconspecificseeddensityrdquo)distancefromthe parent tree and percentage canopy coverWe also includedtree size and total conspecific seedfall at each tree during thestudy (surrogate formedium-scale seed density) as fixed effectvariables because these factorsmay vary between the two for-esttypesandpotentiallyinfluenceseedlingrecruitmentpatterns(Bagchi etal 2011 CurranampWebb 2000) Lastlywe includedinteractions between forest type and the five latter variablesForrandomeffectswesequentiallynestedtheidentitiesofplotswithintransectsandtreestocontrolforpotentialvariationinmi-crotopographythatcouldcausedifferentialgerminationandseed-lingsurvival(Bornetal2015)
Fortheanalysesdescribedabovewebuiltsetsofsub-modelsbasedontheglobalmodelandcomparedmodelsusingAkaikersquos
Information Criterion adjusted for sample size (AICc) (BurnhamampAnderson2002)WeconsideredmodelsfromthelowestAICc until thecumulativemodelweightexceeded95Wethenusedthis95confidencemodelsetasthebasisformodelaveragingandstatisticalinference(BurnhamampAnderson2002)Weconductedall statistical analyses inR (v 321) (RDevelopmentCoreTeam2017)andusedtheglmer function in thepackageldquolme4rdquo (BatesMaumlchler Bolker ampWalker 2015) to fit all GLMMs the packageldquocoxmerdquo(Therneau2015)tofitsurvivalmodelsandthepackageldquoMuMInrdquo(Bartoń2016)formodelselectionandaveraging
3emsp |emspRESULTS
31emsp|emspImpact of logging on seed crop size
ThefivemostparsimoniousmodelswithacumulativeAICcweightof100(Supporting informationTableS2) indicatedthat foresttypedistancefromthefocaltreetreesizeandinteractionsbe-tweenforesttypeandtheothervariableshadsupportinexplain-ingvariationinD lanceolataseedcropsizeanddispersalpatternsConsistentwithprediction1theseedcroptendedtobesmallerin logged forest than in unlogged forest evenwhen accountingfor tree size (Figure3a Table1a)Over ~3months (85days)wecollected2105(n=168traps)and718(n=144traps)seedsinun-loggedandloggedforestrespectivelyTheaverageseeddensity(plusmn1SE) inunloggedforestwas1252(plusmn099)seedsm2comparedwith498(plusmn048)seedsm2inloggedforestThenumberofseedsdeclinedwithincreasingdistancefromthefocaltreesinbothfor-est types (Figure3bTable1a)Consistentwithpatternsof localseed dispersal (Itoh etal 1997) only 06of all trapped seedslanded at 32m in unlogged forest and none in logged forestLarger trees tended toproducemoreseeds inboth forest types(Figure3cTable1a)althoughtreesinloggedforestweresmallerthanthoseinunloggedforest(SupportinginformationFigureS1)Wefoundnoevidenceforoverdispersion(SupportinginformationTableS3)
F IGURE 3emspTherelationshipbetweenD lanceolataseeddensityand(a)foresttype(b)distancefromfocaltreesineachforesttypeand(c)treesizeineachforesttypeErrorbarsandtheshadedregionsofthecurvesarethepredicted95confidenceintervals
(a) (b) (c)
emspensp emsp | emsp8237PILLAY et AL
32emsp|emspImpact of logging on the predation of seeds and seedlings
Over3monthswerecordedanoverallseedandseedlingpredationrate of 866 and 836 in unlogged (n=1423 seeds 140 naturalplots)andlogged(n=646seeds120naturalplots)forestrespec-tivelyAsmallnumberofseeds(unloggedforest5loggedforest8)diedofdesiccationConsistentwithprediction2therewasashiftinthefunctionalroleofseedpredatorsawayfromnon-vertebratesto-wardvertebratesinloggedforest(Figure4ab)Inthenaturalplotsthe log odds of a seedseedling being depredated by vertebrates(relativetonon-vertebrates)werehigherinloggedforestthaninun-loggedforest(βlogged079SE05095CIminus028to185Figure4aSupportinginformationTableS4)Furthersupportingprediction2the logoddsofseedandseedlingpredationwere lower intheex-perimentalexclosureplotsthaninthecontrolplotsinloggedforest(βlogged-exclosureminus210SE05795CIminus343 tominus097Figure4b)In contrast the effect of exclosure treatments on seed predationtendedtobeweakerinunloggedforest(βunlogged-exclosureminus102SE 08895CIminus290to089Figure4bSupportinginformationTableS5)
33emsp|emspImpact of logging on density- dependent germination and seedling survival
We monitored the germination and survival status of seeds thatwerealiveinthenaturalplotsatthefirstcensus(603and227seedsin unlogged and logged forest respectively) until the end of thestudy The sixmost parsimoniousmodelswith a cumulativeAICcweightof97(SupportinginformationTableS6)indicatedthatfor-est type conspecific seed density distance from the parent treeseedfall tree size canopy cover and interactions between foresttypeandtheothervariableshadsupport inexplainingvariation inseedgerminationSeedsfacedgreaterhazard(iehigherprobabilityofmortality) inloggedforestthaninunloggedforest(Table1b)as471ofseedsfailedtogerminateinloggedforestcomparedwith08 in unlogged forestHigher conspecific seed densitywas as-sociatedwithlowerseedmortalityinunloggedforestandthisrela-tionshipalsotendedtoapplyinloggedforest(Figure5aTable1b)With increasingdistancefromparenttreesseedmortalitytendedto increase in both forest types but this relationshipwasweakerin logged forest (Figure5b Table1b) Higher seedfall and largertreesizetendedtobeassociatedwithlowerseedmortalityinbothforest types (Figure5cdTable1b)With increasing canopy coverseedmortality tended to increase inboth forest types (Figure5eTable1b)
Forexplainingvariationinseedlingsurvivalthetwomostparsi-moniousmodelswithacumulativeAICcweightof99(SupportinginformationTableS7) indicated that forest type conspecific seeddensity distance from the parent tree seedfall tree size canopycoverandinteractionsbetweenforesttypeandtheothervariableshad support Of the seeds that germinated seedlings tended tohavelowerprobabilityofmortalityinloggedforestthaninunlogged
forest(Table1c)as817ofgerminatedseedlingssurviveduptotheendofthestudyinloggedforestcomparedwith311inunloggedforestHigherconspecificseedlingdensitytendedtobeassociatedwithhigherseedlingmortality inunloggedforestbut inconsistentwith prediction 3 this relationship was reversed in logged forest(Figure5f Table1c) With increasing distance from parent treesseedlingmortalityincreasedinunloggedforestbutthisrelationshiptendedtobereversedinloggedforest(Figure5gTable1c)Higherseedfall tended tobe associatedwithhigher seedlingmortality inunloggedforestbutthisrelationshipalsotendedtobereversedinloggedforest(Figure5hTable1c)Likegerminationlargertreesizetendedtobeassociatedwithlowerseedlingmortalityinbothforesttypesandthisrelationshipwasstrongerinloggedforest(Figure5iTable1c)With increasingcanopycoverseedlingmortalitytendedtoincreaseinunloggedforestbutthisrelationshiptendedtobere-versedinloggedforest(Figure5jTable1c)
4emsp |emspDISCUSSION
Ourresultsdemonstratehowmultiplestagesoftheseedlingrecruit-mentprocessofacanopytreespeciesmaybealteredwhentropicalforestsaredegradedbyintensiveldquoselectiverdquologgingConsistentwithourpredictions the remaining reproductive trees in logged forestproducedamarkedlysmallerseedcropthanthetreesinunloggedforestevenafteraccountingfortreesizeandthefunctionalroleofvertebratesinseedpredationincreasedinloggedforestwhilethatof non-vertebrates declined The strength of density-dependencein dipterocarpsmay change frompositive to negative at differentlife stages (Blundell amp Peart 2004 Curran ampWebb 2000) Thisappearedtobethecase inunloggedforestwheregermination in-creasedwithlocal-scaleconspecificseeddensitypossiblybecausepredatorsweresatiatedbythehighmast-fruitingseeddensitiesbutseedlingsurvivaltendedtodecline(Figure5afTable1bc)HoweverinconsistentwithourpredictionofstrongerNDDinloggedforestgermination and especially seedling survival increasedwith local-scaleconspecificseeddensitywhichsuggeststhatloggingmayhaveaffectedpredator-mediatedNDDduringtheseed-to-seedlingtran-sitionbottleneck inD lanceolata Importantlyourfindingsappliedtoamast-fruitingyearwhenmostdipterocarprecruitmentoccurs(CurranampLeighton2000Janzen1974)suggestingthat intensiveloggingmaypotentiallyaffectlong-termpopulationdynamicsofD lanceolataOur findings add to knowledge of how ecological pro-cesses responsible for themaintenanceofbiodiversitymaybeaf-fectedbylogging(DarrigodosSantosampVenticinque2018Ewersetal2015Schleuningetal2011Woodcocketal2013)
Increasing edaphic and drought stress in reproducing treesin logged forest may have contributed to the reduced seed crop(Curran etal 1999 Hardwick etal 2015) The consequences ofseed limitation in logged forests for sapling and ultimately adulttree recruitment remain largelyunexploredbutmaybedetrimen-tal for long-term tree population dynamics (Caughlin etal 2015)Changes in the functional roles of non-vertebrate seed predators
8238emsp |emsp emspensp PILLAY et AL
relativetovertebratesinloggedforestmaybedrivenbynumericalchanges inpredatorabundanceacrossgroups (Ewersetal2015)The altered microclimatic conditions in logged forests are likelyhostile to populations of insect seed predators and fungal patho-gens(Ewersetal2015Hardwicketal2015)Converselylogged
forestsmayprovideincreasedresourceavailabilityforrodentseedpredatorsandthusbenefittheirpopulations(Ewersetal2015)
Theuniqueecologyofmast-fruitingandtheimpactthisphenom-enonmayhavesustainedinloggedforestmayexplainthecomplexdensity-dependent patterns of germination and seedling survival(Figure5af)On theonehand in unlogged forest predator satia-tionmayhavebeenoccurringatthehighseeddensitiesduringthemast(Janzen1970)aspotentiallysupportedbyourfindingthatger-minationtendedtoincreasewithhigherseedfall(Figure5cBagchietal2011CurranampWebb2000)Indeedmast-fruitinghasbeenhypothesizedtobeanevolutionaryresponsetodensity-dependentmortality factors allowing seeds to escape predation by satiatingseedpredators (Janzen19701974)Ontheotherhand in loggedforesttheconcentratedseeddensitiesunderspatiallyisolatedadulttreesmayallowNDDtooperate(Bagchietal2011CurranampWebb2000)Howeverourfindingsofincreasedgerminationandespeciallyseedlingsurvivalwithhigherconspecificseeddensityinloggedfor-est(Figure5afTable1bc)werecontrarytotheexpectationsunderNDDandmaybeassociatedwiththediminishedfunctionalroleofnon-vertebrate seedpredators in logged forest (Figure4)NDD isprimarily driven by host-specific insect seed predators and fungalpathogenswhichtendtoconcentrateamongthehigh-seedseedingdensitiesunderthecrownsofparenttreestherebycausinghighermortalitywhere densities are higher (Bagchi etal 2014 Connell1971 Janzen 1970) These non-vertebrate seed predators andpathogensmaybedeclining in logged forests (Ewers etal 2015)andtheirecologicalroleinmaintainingNDDmaybediminishedIncontrastthetendencyofvertebratestoforageoverlargeareasmayrender predation-relatedmortality to bemore spatially heteroge-neousrelativetoseedseedlingdensities(SwamyampTerborgh2010)
Wenotethatseedcropsizegerminationandseedlingsurvivaltendedtoincreaseforlargertreesinbothforesttypes(Figures3c5di)Thissuggeststhatselectiveloggingpracticesthatharvesttim-ber at sustainable rates and followsilviculturalpracticesdesignedtominimizedamagetotheresidualstand(Asneretal2009Martinetal2015Putzetal2012)arecriticaltopreventseedlingrecruit-mentfailure indipterocarpforestsSeedgerminationandseedlingsurvivalofD lanceolatatendstobepositivelyassociatedwithlightavailability (Itoh etal 1995) which likely explains why seed andseedling mortality tended to increase with higher canopy cover(Figure5ej)
41emsp|emspCaveats and limitations
OurstudyincludedsevenandsixD lanceolatatreesasindepend-ent experimental units in unlogged and logged forests respec-tively (cfBagchietal2011HolbrookampLoiselle2009Poulsenetal 2012) The spatially clumped distributions of most adultfruiting individuals inunlogged forestand the fewspatially scat-teredadultdipterocarpsremaininginloggedforest(ofallspeciesD lanceolata was the most abundant at seven individuals) pre-cludedadditionalreplicationatthelevelofindividualtreeswithinforesttypeThesparsenumberofadultdipterocarpsinthelogged
TABLE 1emspModelaveragedestimatesexplainingvariationin(a)seedcropsize(b)germinationand(c)seedlingsurvival(upto3monthsafterseedfall)ofD lanceolatainrelationtothepredictorvariablesthatweresupportedbyAICc-basedmodelselectioncriteria(SupportinginformationTablesS2S6S7)
Response and predictor variables Estimate (SE) 95 CI
(a)Seedcropsize
Intercept 300(029) 240ndash352
Loggedforest minus080(048) minus172ndash007
Distance minus013 (001) minus014tominus011
Loggedforesttimesdistance minus001(001) minus005ndash001
Treesize 006(014) minus018ndash060
Loggedforesttimestreesize 001(010) minus054ndash080
(b)Germination
Logged forest 468 (362) 269ndash1096
Conspecific seed density minus271 (238) minus744tominus075
Logged foresttimesconspecific seed density
265 (235) 105ndash723
Distance 003(018) minus062ndash133
Loggedforesttimesdistance minus002(016) minus134ndash091
Seedfall minus084(157) minus602ndash104
Loggedforesttimesseedfall 024(149) minus422ndash1428
Treesize minus018(098) minus639ndash329
Loggedforesttimestreesize minus014(108) minus1072ndash474
Canopycover 001(032) minus217ndash255
Loggedforesttimescanopycover 015(084) minus155ndash775
(c)Seedlingsurvival
Loggedforest minus710(403) minus1500ndash081
Conspecificseedlingdensity 030(015) minus001ndash060
Logged foresttimesconspecific seedling density
minus170 (043) minus255tominus086
Distance 015 (009) 002ndash032
Logged foresttimesdistance minus104 (067) minus231 tominus012
Seedfall 003(058) minus119ndash126
Loggedforesttimesseedfall minus203(307) minus863ndash389
Treesize minus003(096) minus206ndash199
Logged foresttimestree size minus316 (205) minus706 tominus033
Canopycover 027(028) minus024ndash087
Loggedforesttimescanopycover minus034(110) minus271to191
NotesResultsforseedcropsizerepresentcoefficients(log-scale)esti-matedwithgeneralizedlinearmixedmodelsResultsforgerminationandseedling survival represent loghazardsestimatedwithCox regressionmixed-effectssurvivalmodelsEstimatesinitalicsindicatethatthe95confidenceintervalsdidnotoverlapzerosuggestingastrongeffectofthepredictorvariableonthecorrespondingresponsevariable
emspensp emsp | emsp8239PILLAY et AL
forestisareflectionofthepopulationreductionmanytimbertreespeciesaresubjected toafter intensiveselective logging (Martinetal2015)
The variable density of adultD lanceolata trees between un-logged and logged forests may introduce confounding negativedensity-dependentneighbourhoodeffectsonseedlingrecruitment(BlundellampPeart2004StollampNewbery2005)PreviousresearchontheDipterocarpaceaesuggeststhatneighbourhoodeffectsmayoccurwhenconspecificadultsarewithin20mofeachother(StollampNewbery2005)Ourrequirementofnon-overlappingseedshad-owsbetweenfocaltreesensuredthattreeswereseparatedbyatleast40mTherelativelylargerdistancebetweenthefocaltreesinourstudycomparedwiththethresholddistanceof20matwhichneighbourhoodeffectsmayoccur(StollampNewbery2005)shouldthusservetominimizethispotentialconfoundingfactor
Inanalyzingagentsofseedandseedlingpredationwedidnotdistinguishbetweenthedifferentprocessesofseedlingpredation
andherbivoryOftheseedlingsthatwerealiveinthenaturalplotsat the end of the study 017 and 176 showed signs of leafdamagetypicalofinsectherbivory(ColeyampBarone1996)inun-loggedandloggedforestsrespectively Intheexperimentalandpairedcontrolplotsthepercentageofseedlingswithsignsofleafdamage fromherbivorywas similarly small (061and065 inunloggedand logged forest respectively)Thusobservedseed-lingherbivoryrateswerelowAlonger-termstudymayrevealal-teredseedlingherbivoryrateswithlogging(Darrigoetal2018)particularly because herbivorous insect biomass was found toincrease with logging (Ewers etal 2015) Our study examinestheeffectsofintensiveselectiveloggingontheseed-to-seedlingtransitionphaseofacanopydipterocarpHoweverour findingsmaynot represent the fateofseedlingsovera longer timespanbecause ecological changes caused by logging (eg herbivory)could continue to impact the survival of seedlings beyond theseed-to-seedlingtransitionbottleneck(Caughlinetal2015)
F IGURE 4emspTheoddsofpredationofD lanceolataseedsbyvertebratesrelativetonon-vertebratesin(a)naturalplotsand(b)experimental(vertebrateexclosures)andpairedcontrolplotsinunloggedandloggedforestErrorbarsrepresent95confidenceintervals
(a) (b)
F IGURE 5emspTherelationshipsbetweenD lanceolataseedgermination(toppanel)seedlingsurvival(bottompanel)and(af)conspecificseedseedlingdensity(bg)distancefromtheparenttree(ch)seedfall(di)treesizeand(ej)canopycoverinunloggedandloggedforests
(a) (b) (c) (d) (e)
(f) (g) (h) (i) (j)
8240emsp |emsp emspensp PILLAY et AL
WedidnotmanipulatedensityanddistanceindependentlyOuruseof seeddensity gradientsnaturally generatedby thedistancegradient can identify density-dependent patterns of seedling re-cruitment (Harms etal 2000Webbamp Peart 1999)However intheabsenceofexperimentalmanipulationofdensityanddistanceeffects independent of each other our ability to understand thecauses underlying observed patterns of density-dependence inunloggedand logged forests is limited (SwamyampTerborgh2010)Futurestudiesshouldleveragemanipulativeexperimentsforanu-ancedunderstandingof the causes underlying alteredpatterns ofseedling recruitment in the face of anthropogenic disturbances(FreckletonampLewis2006)
5emsp |emspCONCLUSION
We found that for Dryobalanops lanceolata a dipterocarp spe-ciesendangeredby thecommercial timber trade (Ashton1998)multiple stages of seedling recruitment were altered in selec-tively logged forest compared with unlogged forest during amast-fruiting year Future studies should leverage broader log-ging gradients additional species and experimental approachesover longer time frames (Bagchietal2011Martinetal2015Riuttaetal2018Struebigetal2013SwamyampTerborgh2010)to quantify the thresholds of logging intensity abovewhich theecologicalprocessofseedlingrecruitmentmayunravelWehigh-lighttheimportanceofunderstandingtheimpactsofdisturbancessuch as logging on ecological processeswhich can complementnumericalassessmentsofbiodiversitytounmaskimpactsthatmayotherwiseremainhidden
ACKNOWLEDG MENTS
We thank Yayasan Sabah BentaWawasan Sdn Bhd the SabahBiodiversity Council the Sabah Forestry Department theMaliauBasin Management Committee the State Secretary Sabah ChiefMinisterrsquosDepartmenttheMalaysianEconomicPlanningUnitandtheRoyalSocietySouthEastAsiaRainforestResearchPartnershipfor granting permits Our fieldwork was funded by grants fromthe Rufford Small Grants Foundation IDEAWild the Institute ofFoodandAgriculturalSciencesandtheTropicalConservationandDevelopmentProgramattheUniversityofFloridaWethankRyanGray andMinSheng Khoo for coordinating field logistics MainusTausong JeffryAminMohdYusufDidin (Roy)RismanAjangandMelvin Teronggoh for assistance during fieldwork Magat JaparandJeffryAminfor identifyingtreesseedsandseedlingsJeffreyHostetler forhelpwith survival analysis andEmilioBrunaTrevorCaughlin David Newbery and one anonymous reviewer for con-structivecommentsthatgreatlyimprovedthemanuscript
CONFLIC T OF INTERE S T
Nonedeclared
AUTHOR CONTRIBUTIONS
RPconceivedthisstudyRPandRJFraisedthegrantsforfieldworkRPBALRJFandHBdesignedthemethodologyRPcollectedthedataandperformedallstatisticalanalysesRPandFHledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandprovidedfinalapprovalforpublication
DATA ACCE SSIBILIT Y
DatacanbeaccessedthroughtheDryadDigitalRepositoryhttpsdoiorg105061dryaddk4t694 (Pillay Hua Loiselle Bernard ampFletcher2018)
ORCID
Rajeev Pillay httporcidorg0000-0002-7116-6855
R E FE R E N C E S
AshtonP (1998)Dryobalanops lanceolatahttpwwwiucnredlistorgdetails331640(accessed11March2015)
Asner G P Rudel T K Aide T M Defries R amp Emerson R(2009) A contemporary assessment of change in humid trop-ical forests Conservation Biology 23 1386ndash1395 httpsdoiorg101111j1523-1739200901333x
BagchiRGalleryREGripenbergSGurrSJNarayanLAddisCEhellipLewisOT(2014)Pathogensandinsectherbivoresdriverain-forestplantdiversityandcompositionNature50685ndash88httpsdoiorg101038nature12911
Bagchi R Philipson C D Slade E M Hector A Phillips SVillanueva J F hellip Press M C (2011) Impacts of logging ondensity-dependentpredationofdipterocarpseedsinaSouthEastAsian rainforestPhilosophical Transactions of the Royal Society B Biological Sciences 366 3246ndash3255 httpsdoiorg101098rstb20110034
Bartoń K (2016) MuMIn Multi-model inference R package version 1156
BatesDMaumlchlerMBolkerBMampWalkerSC(2015)Fittinglinearmixed-effectsmodelsusing lme4Journal of Statistical Software67httpsdoiorg1018637jssv067i01
BlundellAGampPeartDR(2004)Density-dependentpopulationdy-namicsofadominantrainforestcanopytreeEcology85704ndash715httpsdoiorg10189001-4101
BornJBagchiRBurslemDNilusRTellenbachCPluessARampGhazoulJ(2015)DifferentialresponsesofdipterocarpseedlingstosoilmoistureandmicrotopographyBiotropica4749ndash58httpsdoiorg101111btp12180
BrunaEM (1999) Seedgermination in rainforest fragmentsNature402139httpsdoiorg10103845963
BurnhamKPampAndersonDR(2002)Model Selection and Multimodel Inference A Practical Information-Theoretic ApproachNewYorkNYSpringer-Verlaghttpsdoiorg101007b97636
Caughlin T T Ferguson J M Lichstein J W Zuidema P ABunyavejchewinSampLeveyD J (2015)Lossofanimal seeddis-persalincreasesextinctionriskinatropicaltreespeciesduetoper-vasivenegativedensitydependenceacross life stagesProceedings of the Royal Society B Biological Sciences28220142095httpsdoiorg101098rspb20142095
ChambersJCampMacMahonJA (1994)Adayinthe lifeofaseedMovementsandfatesofseedsandtheirimplicationsfornaturaland
emspensp emsp | emsp8241PILLAY et AL
managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
emspensp emsp | emsp8233PILLAY et AL
2emsp |emspMATERIAL S AND METHODS
21emsp|emspStudy area
Weconductedfieldworkintwodipterocarp-dominatedforestsitesspaced 65km apart in Sabah Malaysian Borneo These sites arepart of the experimental design of the Stability of Altered ForestEcosystems(SAFE)Project(Ewersetal2011)andencompasspri-maryforestwithintheMaliauBasinConservationArea(MBCA)andrepeatedlyloggedforestwithintheKalabakanForestReserve(KFR)aloggingconcessionintheYayasanSabahForestManagementAreaOverallthelogginggradientencompassedwithintheSAFEexperi-mental design resembles the pattern of habitat conversion acrossthewiderregion(Ewersetal2011Struebigetal2013)
TheforestatMBCA(a5884km2protectedarea)representsthenearest topographicallymatchedprimary forest to the logged for-est inKFR(Ewersetal2011Struebigetal2013)Thetwositesarealsosimilar intermsofsoilnutrientprofilesandphysicalprop-erties(Riuttaetal2018)TheMBCAservesastheunloggedcon-trolsiteof theSAFEProject (Ewersetal2011)Twoof thethreecontrolblocks atMBCA (hereafter ldquounlogged forestrdquo) (OG1OG2)haveneverbeenloggedwhilethethird(OG3)waslightlyloggedinthe1970sand1990s (seeEwersetal2011)AspartoftheSAFEProjectexperimentalforestfragments(110100ha)arebeingcre-atedinKFR(Ewersetal2011)PriortothisexperimentKFRwassubjectedtomultiplerotationsofloggingthefirstofwhichbeganinthe1970s(Chong2005Fisheretal2011)Commerciallyvalu-abletreesgt60cmdiameteratbreastheight(DBH)wereextractedand11296m3haoftimberwasremoved(Fisheretal2011)Thesecond rotation commencing in the 2000s (Chong 2005 Fisheretal2011)encompassedthreeroundsduringwhichtreesgt40cmDBH were targeted (Fisher etal 2011 Struebig etal 2013) Avolumeof25872232 and1816m3haof timberwasextractedduringeachroundrespectively(YayasanSabahunpublisheddata)Logging ended in 2007ndash2008 (Fisher etal 2011) by which time17931m3haof timberwascumulatively removed (Struebigetal
2013)Extensivecollateraldamagetoforeststructurealsooccurredduetotheestablishmentofskidtrailsaccessroadsandlog-landingareas (WearnRowcliffeCarboneBernardampEwers2013)Thustheloggingintensitywasaround45timesthethresholdoflt40m3habeyondwhichresidualstanddamagesurpassesthe25ndash30limitconsidered sustainable (Martin etal 2015) The six experimentalblocks(AndashF)atSAFE(hereafterldquologgedforestrdquo)(Ewersetal2011)comprise a heterogeneous landscape that has been subjected tovaryingintensitiesandtimingsoftimberextraction
22emsp|emspStudy species
Dryobalanops lanceolataBurckisanemergenttreethatcangrowupto80mhigh(Soepadmoetal2002)EndemictoBorneoitiswide-spread and common in the statesof Sabah andSarawak growinginmixed-dipterocarp forestonclay-richsoils (SoepadmoampWong1995Soepadmoetal2002)Thesaplingsareshadetolerant(ItohYamakuraOginoampLee1995)andcansurvivemanyyearsexpand-inghorizontallyuntilacanopygapopensup(Soepadmoetal2002)It is ahardwoodspeciesvalued for its construction timber that issoldunder the tradenameKapur (Soepadmoetal 2002)Due tocommercialharvestingandhabitat loss it isnowrareoutsidepro-tectedareasand isclassifiedasEndangered(IUCNRedListv23Ashton 1998) Like other dipterocarps its winged seeds are dis-persedbygyration (Figure1)andmostly fall incloseproximity tothecrownoftheparenttree(ItohYamakuraOginoLeeampAshton1997)Itsseedsandseedlingsareattackedbyfungalpathogens(per-sonal observation)insectsandvertebratessuchasbeardedpigs(Sus barbatus)andvariousspeciesofrodents(Itohetal1995)
23emsp|emspStudy design
Weconductedfieldworkduringamast-fruitingeventthatoccurredin2014 InJuneandJulyprior to thecommencementofseedfallwe surveyed ~2146km of forest trails that passed through thediametersof the110 and100ha ldquofragmentsrdquoofBlocksABD
F IGURE 1emspDryobalanops lanceolataisanendangereddipterocarpendemictoBorneoTheseedsarewinddispersedandmostlyfallneartheparenttreeLeftAmatureseedgerminatingD lanceolataseedshavefivewingsandaregreenwhentheyfallfromthetreebutturnpinkupongerminationwithin5ndash7daysofdispersalCenterMarkedseedlingsinanaturalplotRightSeedlingsinanexperimental(vertebrateexclosure)plotPhotocreditsRajeevPillay
8234emsp |emsp emspensp PILLAY et AL
E andF in the logged forest andwere able to locate only sevenadultD lanceolatatreesinactivefruitingcondition(withinBlockEtwotreeswithinandaroundBlockFfivetrees)OneofthetreesinBlockEwaslt40mfromtheotherreproductiveconspecificWeremovedthis individual fromthisstudytoensurenon-overlappingseedshadowssincepriorworkonD lanceolatainSarawakBorneo(Itohetal1997)indicatesthatallseedsaredispersedlt40mfromthe parent treeWe included the remaining six individuals in thisstudyThusthesparsenumberofadultconspecificsinactivefruit-ingconditiondictatedoursamplesizeatthelevelofindividualtreesIn the unlogged forest sitewe surveyed approximately 65kmofforesttrailseachinBlocksOG1andOG2andlocated15ndash20(OG1)and20ndash25(OG2)adultD lanceolatatreesinactivefruitingcondition(weexcludedOG3fromthisstudydueto its logginghistory)TheseedshadowsofalltreesinOG1overlappedwiththoseofatleastoneotherconspecificadultThereforeweselectedsevenindividu-alsinOG2whoseseedshadowsdidnotoverlapwiththoseofotherreproductiveconspecificsWeconsideredeachindividualfocaltreeasanexperimentalunitresultinginsevenandsixreplicatesatthelevelofindividualtreesinunloggedandloggedforestrespectivelyIndividualtreesareoftenusedasexperimentalunitsinseeddisper-salandseedlingrecruitmentstudiesandmaybeconsidered inde-pendentsamplesiftheirseedshadowsdonotoverlapwiththoseofotherconspecifics (Bagchietal2011HolbrookampLoiselle2009Poulsenetal2012)
Thesevenfocaltreesinunloggedforestwere303mapartonaveragewith the smallest pairwise distance between two treesbeing40mThesixfocaltreesinloggedforestwere1690mapartonaveragewiththesmallestpairwisedistancebetweentwotreesbeing244mandcoverconsiderable landscapeheterogeneity interms of logging intensity and time since logging (Wearn etal2013)Onaverageourfocaltreeswerearound56timesfurtherapart from each other in logged forest than in unlogged forestwhichpotentiallyindicatestheintensityofextractionifD lance-olatapopulationdensitiesweresimilar inbothforesttypespriortologging
Wesetupfour32mtransectsextendingfromthebaseofeachfocaltreewiththefirsttransectorientedalongarandomcompassdirection and each subsequent transect at 90deg from the previous(Figure2)We constrained transect length to 32m because priorwork indicated that few seeds reached this distance (Itoh etal1997)AlongeachtransectweusedseedtrapstoquantifytheseedcropandseeddispersaldistancesettingthemupsoonafterseedfallcommencedinearlyAugust2014Wedeployedtheseedtrapsonalog2scaleat124816and32mdistances(n=24seedtrapstreeFigure2)Eachtrapwasa1times1mnylonmeshnetsuspendedby1-mtallPVCpipesateachcornerThevalidityofourdatareliesontheassumptionthatourfocaltreeshadnon-overlappingseedshadowsSince995of all seeds fell into the seed trapswithin16m fromtheirrespectiveparenttrees(seeSection3)adistancethat is lessthanhalfoftheminimumdistancebetweenanyofourfocal trees(ie40m)theseedsweincludedinthisstudyshouldbepredomi-nantlyifnotentirelyfromtheirrespectiveparenttrees
Wemonitoredseedpredationanddensity-dependentpatternsofgerminationandseedlingsurvivalof individualseedsthatnatu-rally dispersed into individual 1times1m unmanipulated monitoringplots (hereafter ldquonatural plotsrdquo) We thus utilized the conspecificseedseedlingdensitygradientnaturallygeneratedbythedistancegradient forourassessmentofNDDWeplacednaturalplots2mtotheleftoftheseedtrapsalongeachtransectat24816and32m distances (n=20 natural plotstree Figure2) Additionallyaround 1month after the commencement of seedfall we set upvertebrate-exclosure plots (hereafter ldquoexperimental plotsrdquo) andpairednon-exclosureplots(hereafterldquocontrolplotsrdquo)totestfortherelativecontributionofvertebratesversusinsectsandfungitoseedpredationWeplacedexperimentalandcontrolplotsat2and32mdistancesalongone randomlyselected transectateach focal tree(n=2 plot pairstree Figure2)At 32mweplaced eachplot pair2mfromeachotherandontherightsideofthecorrespondingseedtraprandomlyassigningtherelativepositionofexperimentalversuscontrolplots(iewhichplotwasplacedadjacenttothecorrespond-ingseedtrap)At2mduetolimitedspacenearthebaseofthefocaltreeweplacedoneplotontherightofthecorrespondingseedtrapandthepairedplotatthecorrespondingpositionalongthediago-nallyoppositetransectrandomlyassigningtherelativepositionofexperimentalversuscontrolplots (Figure2)Dueto logisticalcon-straintsweomittedoneof themost remote focal trees in loggedforestinthiscomparisonandinsteadsetuptwoadditionalplotpairsinthesamewayaroundanotherofourfocaltreeswhichwasmore
F IGURE 2emspStudydesignshowingseedtraps(at124816and32mdistances)naturalplots(at24816and32mdistances)andpairedexperimental(vertebrateexclosures)andcontrolplots(at2and32mdistances)alongfour-32mtransectsfromthebaseoffocalD lanceolatatreesSeedtrapsnaturalandcontrolplotswere1times1minareaExperimentalplotswere1times1times05mFigurenottoscale
12 4 8 16 32
Focal treeSeed trapNatural plotExperimental plotControl plot
emspensp emsp | emsp8235PILLAY et AL
accessible Experimental plotswere 1times1times05mwith the exclo-suremade fromsteelwireof127times127cmmeshsize toexcludeallvertebrateseedpredatorsbutnotinsectseedpredatorsorfungalpathogens(Figure1)Controlplotswereopentoallseedpredatorsandpathogens
ForthepairedexperimentalandcontrolplotsweaddedD lance-olataseedsatpredefineddensities~1monthaftercommencementof seedfall and thereafter continuously removed all conspecificseedsthatfellintothecontrolplotsthroughoutthedurationofthestudyWeused a seeddensity of 5seedsm2 for thepairedplotsat2mdistancesand50seedsm2 forthoseat32mdistancesForseeding the plots we collected intact (ie no visible evidence ofpredatorattack)matureseedsfromaround20non-focalD lanceo-latatreesinunloggedforestWethoroughlymixedtheseseedsandplacedthemonthesoilsurfaceinaregulargridtomimicthenaturalseedfallpatterninwhichseedsgyratefromtheparenttreesandlandonthegroundWethusdistributed770seeds(n=28experimentalandpairedcontrolplots)ineachforesttypeWenotethatthispartofthestudyaimstoprovideonlyasupportingassessmentoftherel-ative importanceofvertebrateandnon-vertebrateseedpredatorsinunloggedandloggedforestsWedidnotattempttomanipulatedensity anddistance independentlydue to logisticaldifficulties incollecting and sowing additional seeds a time-sensitive undertak-ingbecauseoftherapidityatwhichseedsgerminatetogenerateaspectrumofseeddensities thatwouldreflectscenariosunderun-loggedandloggedconditions(cfBagchietal2011Poulsenetal2012)
24emsp|emspData collection
We collected seeds from the traps at two census intervals be-tween12Augustand4Novemberinloggedforestandbetween1Septemberand22October inunloggedforestWemonitoredthefateofeveryseeduponinitiatingthenaturalplots(atthesameinter-valsastheseedtraps)untiltheendofthestudyWetaggedallseedswithnumberedplastictagsstapledtotheirwings(Figure1)andcon-tinuedtaggingseedsthatnewlyfell intothenaturalplotsAteachcensusintervalwerecordedthenumberofseedsthatsurvivedanddiedineachplotForsurvivingseedswerecordediftheywereger-minatingandsubsequentlywhether they recruited into seedlingsWealsoscoredeachseedintooneofthefollowingcategories(afterBagchietal2011)intact(novisiblesignsoffungalinsectorverte-brateattack)germinated(definedasemergenceoftheradicleItohetal1995)seedling(ge5cmtallexpandedtrueleaves)vertebratedepredated(partiallyeatengnawedorremoved)insectdepredated(withentryexitholes) fungusdepredated(withfungalsporesmy-celia)Wenote that the seeds falling into the natural plotswouldlikely be exposed to both pre-dispersal and postdispersal insectpredators(Bagchietal2011)Wewerecarefultoclassifydepreda-tionstatusonthebasisofthepredatorthatweinitiallyrecordedtohaveattackedtheseedseedling(LewisampGripenberg2008)Thusaseedwithinsectentryexitholesattheinitialcensusthatwassub-sequentlypartiallyeatenorremovedbyvertebrateswasscoredas
predatedbyinsectsDuetothedifficultyinascertainingtheinitialpredatorbetweeninsectsandfungalpathogenswecollapsedthemintothenon-vertebratecategoryWethususedtwopredatorcat-egoriesvertebrateversusnon-vertebrate
WemeasuredasetofecologicalcovariatesthatcanpotentiallyinfluencevariousstagesofseedlingrecruitmentandthusshouldbeaccountedforinexaminingtheimpactsofloggingThesecovariatesincludedthreemeasuresoftreesizethataredeterminantsofseedcropsizeanddispersaldistanceDBHheightandcrowndiameter(CousensDythamampLaw2008NorghauerNockampGrogan2011)We also measured percentage canopy cover as a proxy for lightavailabilitywhich in turnmay influencegerminationand seedlingsurvival(Kobe1999)SeeSupportinginformationAppendixS1fordetailsonthesemeasurements
25emsp|emspStatistical analyses
Wefirstusedprincipal-componentsanalysis(PCA)toidentifymajortrends intreesizedataandreducethenumberofvariablesrepre-sentingtreesizeThefirstprincipalcomponent(PC1)waspositivelycorrelatedwithallthreevariablesrepresentingtreesizehadanei-genvaluegt1andexplained764ofthetotalvarianceintreesizedata (Supporting information Table S1) We used the componentscoresgeneratedfromthe loadingsofPC1asasurrogatefor treesizeinfurtherstatisticalanalyses
Wethenusedgeneralizedlinearmixedmodels(GLMMs)toana-lyzetheimpactsofloggingonseedcropsizeanddispersalpatternsusingthenumberofseeds ineachseedtrapastheresponsevari-ableWeusedforesttype(unloggedvslogged)distancefromthefocaltreePC1(hereafterldquotreesizerdquo)andalltwo-wayinteractionsbetween forest type and the other variables as fixed effectsWeincluded individualseedtrapsnestedwithintreesasa random in-terceptinallmodelsWeassumedaPoissonerrordistributionandaloglinkfunctionWetestedforoverdispersionbycalculatingthesumofsquaredPearsonresidualsandcomparing it totheresidualdegreesoffreedomforeachmodel(ZuurIenoWalkerSavelievampSmith2009)
WealsousedGLMMstoanalyzetheimpactofloggingontherelative role of vertebrates versus non-vertebrates inD lanceo-lataseedandseedlingpredationOurobservationsindicatedthatmostseedlingsdiedfrompredation(eguprootedandpartiallycompletelyconsumedremovedbyvertebratescotyledonsofger-minatedseedlingsdestroyedbyinsectsandorfungalpathogens)rather than from leaf damage typically inflicted by herbivores(ColeyampBarone1996)Thereforewepooleddataon seedandseedling predation For the natural plotswe scored each seedseedling as depredated by either vertebrate or non-vertebratepredators and then modeled the probability of a seedseedlingbeingdepredatedbyvertebrates (relative tonon-vertebrates)asa functionof forest typeas the fixedeffectvariableForpairedexperimental and controlplotswecounted thenumberofdep-redated seedsseedlings out of the total number of seeds andthenmodeledtheprobabilityofseedseedlingpredationWeused
8236emsp |emsp emspensp PILLAY et AL
foresttypeandtreatmenttype(experimentalvscontrolplots)asfixedeffectvariablesInbothanalysesofseedseedlingpredationweincludedindividualplotssequentiallynestedwithintransectsandtreesasarandominterceptWeassumedabinomialerrordis-tribution and a logit link functionWe note that nomadic herdsof bearded pigs destroyed our experimental exclosures for fourout of seven trees in unlogged forest (but not in logged forest)between1and19October(~30daysfromtheonsetofseedseed-lingmonitoringintheseplots)Thereforeforunloggedforestweonly considered data from the paired experimental and controlplotsforthethreetreesthatwerenotdepredatedbybeardedpigs(n=330seeds12plots)
WeusedCoxregressionmixed-effectssurvivalmodelstoan-alyzethe impactof loggingongerminationandseedlingsurvivalatthelevelofindividualseedsandseedlingswithdatacollectedfromthenaturalplotsWefirstmodeledseedsurvivaluntilger-minationwithsurvivalmodeledasdailygerminationrateOftheseeds that germinatedwe subsequentlymodeled daily seedlingsurvivaluntil3monthsafterseedfallWeincorporatedseedseed-lingageandusedright-censoring ifaseedseedlingsurvivedbe-yondtheendofthemonitoringperiodForfixedeffectvariablesweincludedforesttypelocal-scale(1m2)conspecificseedseed-lingdensity (hereafter ldquoconspecificseeddensityrdquo)distancefromthe parent tree and percentage canopy coverWe also includedtree size and total conspecific seedfall at each tree during thestudy (surrogate formedium-scale seed density) as fixed effectvariables because these factorsmay vary between the two for-esttypesandpotentiallyinfluenceseedlingrecruitmentpatterns(Bagchi etal 2011 CurranampWebb 2000) Lastlywe includedinteractions between forest type and the five latter variablesForrandomeffectswesequentiallynestedtheidentitiesofplotswithintransectsandtreestocontrolforpotentialvariationinmi-crotopographythatcouldcausedifferentialgerminationandseed-lingsurvival(Bornetal2015)
Fortheanalysesdescribedabovewebuiltsetsofsub-modelsbasedontheglobalmodelandcomparedmodelsusingAkaikersquos
Information Criterion adjusted for sample size (AICc) (BurnhamampAnderson2002)WeconsideredmodelsfromthelowestAICc until thecumulativemodelweightexceeded95Wethenusedthis95confidencemodelsetasthebasisformodelaveragingandstatisticalinference(BurnhamampAnderson2002)Weconductedall statistical analyses inR (v 321) (RDevelopmentCoreTeam2017)andusedtheglmer function in thepackageldquolme4rdquo (BatesMaumlchler Bolker ampWalker 2015) to fit all GLMMs the packageldquocoxmerdquo(Therneau2015)tofitsurvivalmodelsandthepackageldquoMuMInrdquo(Bartoń2016)formodelselectionandaveraging
3emsp |emspRESULTS
31emsp|emspImpact of logging on seed crop size
ThefivemostparsimoniousmodelswithacumulativeAICcweightof100(Supporting informationTableS2) indicatedthat foresttypedistancefromthefocaltreetreesizeandinteractionsbe-tweenforesttypeandtheothervariableshadsupportinexplain-ingvariationinD lanceolataseedcropsizeanddispersalpatternsConsistentwithprediction1theseedcroptendedtobesmallerin logged forest than in unlogged forest evenwhen accountingfor tree size (Figure3a Table1a)Over ~3months (85days)wecollected2105(n=168traps)and718(n=144traps)seedsinun-loggedandloggedforestrespectivelyTheaverageseeddensity(plusmn1SE) inunloggedforestwas1252(plusmn099)seedsm2comparedwith498(plusmn048)seedsm2inloggedforestThenumberofseedsdeclinedwithincreasingdistancefromthefocaltreesinbothfor-est types (Figure3bTable1a)Consistentwithpatternsof localseed dispersal (Itoh etal 1997) only 06of all trapped seedslanded at 32m in unlogged forest and none in logged forestLarger trees tended toproducemoreseeds inboth forest types(Figure3cTable1a)althoughtreesinloggedforestweresmallerthanthoseinunloggedforest(SupportinginformationFigureS1)Wefoundnoevidenceforoverdispersion(SupportinginformationTableS3)
F IGURE 3emspTherelationshipbetweenD lanceolataseeddensityand(a)foresttype(b)distancefromfocaltreesineachforesttypeand(c)treesizeineachforesttypeErrorbarsandtheshadedregionsofthecurvesarethepredicted95confidenceintervals
(a) (b) (c)
emspensp emsp | emsp8237PILLAY et AL
32emsp|emspImpact of logging on the predation of seeds and seedlings
Over3monthswerecordedanoverallseedandseedlingpredationrate of 866 and 836 in unlogged (n=1423 seeds 140 naturalplots)andlogged(n=646seeds120naturalplots)forestrespec-tivelyAsmallnumberofseeds(unloggedforest5loggedforest8)diedofdesiccationConsistentwithprediction2therewasashiftinthefunctionalroleofseedpredatorsawayfromnon-vertebratesto-wardvertebratesinloggedforest(Figure4ab)Inthenaturalplotsthe log odds of a seedseedling being depredated by vertebrates(relativetonon-vertebrates)werehigherinloggedforestthaninun-loggedforest(βlogged079SE05095CIminus028to185Figure4aSupportinginformationTableS4)Furthersupportingprediction2the logoddsofseedandseedlingpredationwere lower intheex-perimentalexclosureplotsthaninthecontrolplotsinloggedforest(βlogged-exclosureminus210SE05795CIminus343 tominus097Figure4b)In contrast the effect of exclosure treatments on seed predationtendedtobeweakerinunloggedforest(βunlogged-exclosureminus102SE 08895CIminus290to089Figure4bSupportinginformationTableS5)
33emsp|emspImpact of logging on density- dependent germination and seedling survival
We monitored the germination and survival status of seeds thatwerealiveinthenaturalplotsatthefirstcensus(603and227seedsin unlogged and logged forest respectively) until the end of thestudy The sixmost parsimoniousmodelswith a cumulativeAICcweightof97(SupportinginformationTableS6)indicatedthatfor-est type conspecific seed density distance from the parent treeseedfall tree size canopy cover and interactions between foresttypeandtheothervariableshadsupport inexplainingvariation inseedgerminationSeedsfacedgreaterhazard(iehigherprobabilityofmortality) inloggedforestthaninunloggedforest(Table1b)as471ofseedsfailedtogerminateinloggedforestcomparedwith08 in unlogged forestHigher conspecific seed densitywas as-sociatedwithlowerseedmortalityinunloggedforestandthisrela-tionshipalsotendedtoapplyinloggedforest(Figure5aTable1b)With increasingdistancefromparenttreesseedmortalitytendedto increase in both forest types but this relationshipwasweakerin logged forest (Figure5b Table1b) Higher seedfall and largertreesizetendedtobeassociatedwithlowerseedmortalityinbothforest types (Figure5cdTable1b)With increasing canopy coverseedmortality tended to increase inboth forest types (Figure5eTable1b)
Forexplainingvariationinseedlingsurvivalthetwomostparsi-moniousmodelswithacumulativeAICcweightof99(SupportinginformationTableS7) indicated that forest type conspecific seeddensity distance from the parent tree seedfall tree size canopycoverandinteractionsbetweenforesttypeandtheothervariableshad support Of the seeds that germinated seedlings tended tohavelowerprobabilityofmortalityinloggedforestthaninunlogged
forest(Table1c)as817ofgerminatedseedlingssurviveduptotheendofthestudyinloggedforestcomparedwith311inunloggedforestHigherconspecificseedlingdensitytendedtobeassociatedwithhigherseedlingmortality inunloggedforestbut inconsistentwith prediction 3 this relationship was reversed in logged forest(Figure5f Table1c) With increasing distance from parent treesseedlingmortalityincreasedinunloggedforestbutthisrelationshiptendedtobereversedinloggedforest(Figure5gTable1c)Higherseedfall tended tobe associatedwithhigher seedlingmortality inunloggedforestbutthisrelationshipalsotendedtobereversedinloggedforest(Figure5hTable1c)Likegerminationlargertreesizetendedtobeassociatedwithlowerseedlingmortalityinbothforesttypesandthisrelationshipwasstrongerinloggedforest(Figure5iTable1c)With increasingcanopycoverseedlingmortalitytendedtoincreaseinunloggedforestbutthisrelationshiptendedtobere-versedinloggedforest(Figure5jTable1c)
4emsp |emspDISCUSSION
Ourresultsdemonstratehowmultiplestagesoftheseedlingrecruit-mentprocessofacanopytreespeciesmaybealteredwhentropicalforestsaredegradedbyintensiveldquoselectiverdquologgingConsistentwithourpredictions the remaining reproductive trees in logged forestproducedamarkedlysmallerseedcropthanthetreesinunloggedforestevenafteraccountingfortreesizeandthefunctionalroleofvertebratesinseedpredationincreasedinloggedforestwhilethatof non-vertebrates declined The strength of density-dependencein dipterocarpsmay change frompositive to negative at differentlife stages (Blundell amp Peart 2004 Curran ampWebb 2000) Thisappearedtobethecase inunloggedforestwheregermination in-creasedwithlocal-scaleconspecificseeddensitypossiblybecausepredatorsweresatiatedbythehighmast-fruitingseeddensitiesbutseedlingsurvivaltendedtodecline(Figure5afTable1bc)HoweverinconsistentwithourpredictionofstrongerNDDinloggedforestgermination and especially seedling survival increasedwith local-scaleconspecificseeddensitywhichsuggeststhatloggingmayhaveaffectedpredator-mediatedNDDduringtheseed-to-seedlingtran-sitionbottleneck inD lanceolata Importantlyourfindingsappliedtoamast-fruitingyearwhenmostdipterocarprecruitmentoccurs(CurranampLeighton2000Janzen1974)suggestingthat intensiveloggingmaypotentiallyaffectlong-termpopulationdynamicsofD lanceolataOur findings add to knowledge of how ecological pro-cesses responsible for themaintenanceofbiodiversitymaybeaf-fectedbylogging(DarrigodosSantosampVenticinque2018Ewersetal2015Schleuningetal2011Woodcocketal2013)
Increasing edaphic and drought stress in reproducing treesin logged forest may have contributed to the reduced seed crop(Curran etal 1999 Hardwick etal 2015) The consequences ofseed limitation in logged forests for sapling and ultimately adulttree recruitment remain largelyunexploredbutmaybedetrimen-tal for long-term tree population dynamics (Caughlin etal 2015)Changes in the functional roles of non-vertebrate seed predators
8238emsp |emsp emspensp PILLAY et AL
relativetovertebratesinloggedforestmaybedrivenbynumericalchanges inpredatorabundanceacrossgroups (Ewersetal2015)The altered microclimatic conditions in logged forests are likelyhostile to populations of insect seed predators and fungal patho-gens(Ewersetal2015Hardwicketal2015)Converselylogged
forestsmayprovideincreasedresourceavailabilityforrodentseedpredatorsandthusbenefittheirpopulations(Ewersetal2015)
Theuniqueecologyofmast-fruitingandtheimpactthisphenom-enonmayhavesustainedinloggedforestmayexplainthecomplexdensity-dependent patterns of germination and seedling survival(Figure5af)On theonehand in unlogged forest predator satia-tionmayhavebeenoccurringatthehighseeddensitiesduringthemast(Janzen1970)aspotentiallysupportedbyourfindingthatger-minationtendedtoincreasewithhigherseedfall(Figure5cBagchietal2011CurranampWebb2000)Indeedmast-fruitinghasbeenhypothesizedtobeanevolutionaryresponsetodensity-dependentmortality factors allowing seeds to escape predation by satiatingseedpredators (Janzen19701974)Ontheotherhand in loggedforesttheconcentratedseeddensitiesunderspatiallyisolatedadulttreesmayallowNDDtooperate(Bagchietal2011CurranampWebb2000)Howeverourfindingsofincreasedgerminationandespeciallyseedlingsurvivalwithhigherconspecificseeddensityinloggedfor-est(Figure5afTable1bc)werecontrarytotheexpectationsunderNDDandmaybeassociatedwiththediminishedfunctionalroleofnon-vertebrate seedpredators in logged forest (Figure4)NDD isprimarily driven by host-specific insect seed predators and fungalpathogenswhichtendtoconcentrateamongthehigh-seedseedingdensitiesunderthecrownsofparenttreestherebycausinghighermortalitywhere densities are higher (Bagchi etal 2014 Connell1971 Janzen 1970) These non-vertebrate seed predators andpathogensmaybedeclining in logged forests (Ewers etal 2015)andtheirecologicalroleinmaintainingNDDmaybediminishedIncontrastthetendencyofvertebratestoforageoverlargeareasmayrender predation-relatedmortality to bemore spatially heteroge-neousrelativetoseedseedlingdensities(SwamyampTerborgh2010)
Wenotethatseedcropsizegerminationandseedlingsurvivaltendedtoincreaseforlargertreesinbothforesttypes(Figures3c5di)Thissuggeststhatselectiveloggingpracticesthatharvesttim-ber at sustainable rates and followsilviculturalpracticesdesignedtominimizedamagetotheresidualstand(Asneretal2009Martinetal2015Putzetal2012)arecriticaltopreventseedlingrecruit-mentfailure indipterocarpforestsSeedgerminationandseedlingsurvivalofD lanceolatatendstobepositivelyassociatedwithlightavailability (Itoh etal 1995) which likely explains why seed andseedling mortality tended to increase with higher canopy cover(Figure5ej)
41emsp|emspCaveats and limitations
OurstudyincludedsevenandsixD lanceolatatreesasindepend-ent experimental units in unlogged and logged forests respec-tively (cfBagchietal2011HolbrookampLoiselle2009Poulsenetal 2012) The spatially clumped distributions of most adultfruiting individuals inunlogged forestand the fewspatially scat-teredadultdipterocarpsremaininginloggedforest(ofallspeciesD lanceolata was the most abundant at seven individuals) pre-cludedadditionalreplicationatthelevelofindividualtreeswithinforesttypeThesparsenumberofadultdipterocarpsinthelogged
TABLE 1emspModelaveragedestimatesexplainingvariationin(a)seedcropsize(b)germinationand(c)seedlingsurvival(upto3monthsafterseedfall)ofD lanceolatainrelationtothepredictorvariablesthatweresupportedbyAICc-basedmodelselectioncriteria(SupportinginformationTablesS2S6S7)
Response and predictor variables Estimate (SE) 95 CI
(a)Seedcropsize
Intercept 300(029) 240ndash352
Loggedforest minus080(048) minus172ndash007
Distance minus013 (001) minus014tominus011
Loggedforesttimesdistance minus001(001) minus005ndash001
Treesize 006(014) minus018ndash060
Loggedforesttimestreesize 001(010) minus054ndash080
(b)Germination
Logged forest 468 (362) 269ndash1096
Conspecific seed density minus271 (238) minus744tominus075
Logged foresttimesconspecific seed density
265 (235) 105ndash723
Distance 003(018) minus062ndash133
Loggedforesttimesdistance minus002(016) minus134ndash091
Seedfall minus084(157) minus602ndash104
Loggedforesttimesseedfall 024(149) minus422ndash1428
Treesize minus018(098) minus639ndash329
Loggedforesttimestreesize minus014(108) minus1072ndash474
Canopycover 001(032) minus217ndash255
Loggedforesttimescanopycover 015(084) minus155ndash775
(c)Seedlingsurvival
Loggedforest minus710(403) minus1500ndash081
Conspecificseedlingdensity 030(015) minus001ndash060
Logged foresttimesconspecific seedling density
minus170 (043) minus255tominus086
Distance 015 (009) 002ndash032
Logged foresttimesdistance minus104 (067) minus231 tominus012
Seedfall 003(058) minus119ndash126
Loggedforesttimesseedfall minus203(307) minus863ndash389
Treesize minus003(096) minus206ndash199
Logged foresttimestree size minus316 (205) minus706 tominus033
Canopycover 027(028) minus024ndash087
Loggedforesttimescanopycover minus034(110) minus271to191
NotesResultsforseedcropsizerepresentcoefficients(log-scale)esti-matedwithgeneralizedlinearmixedmodelsResultsforgerminationandseedling survival represent loghazardsestimatedwithCox regressionmixed-effectssurvivalmodelsEstimatesinitalicsindicatethatthe95confidenceintervalsdidnotoverlapzerosuggestingastrongeffectofthepredictorvariableonthecorrespondingresponsevariable
emspensp emsp | emsp8239PILLAY et AL
forestisareflectionofthepopulationreductionmanytimbertreespeciesaresubjected toafter intensiveselective logging (Martinetal2015)
The variable density of adultD lanceolata trees between un-logged and logged forests may introduce confounding negativedensity-dependentneighbourhoodeffectsonseedlingrecruitment(BlundellampPeart2004StollampNewbery2005)PreviousresearchontheDipterocarpaceaesuggeststhatneighbourhoodeffectsmayoccurwhenconspecificadultsarewithin20mofeachother(StollampNewbery2005)Ourrequirementofnon-overlappingseedshad-owsbetweenfocaltreesensuredthattreeswereseparatedbyatleast40mTherelativelylargerdistancebetweenthefocaltreesinourstudycomparedwiththethresholddistanceof20matwhichneighbourhoodeffectsmayoccur(StollampNewbery2005)shouldthusservetominimizethispotentialconfoundingfactor
Inanalyzingagentsofseedandseedlingpredationwedidnotdistinguishbetweenthedifferentprocessesofseedlingpredation
andherbivoryOftheseedlingsthatwerealiveinthenaturalplotsat the end of the study 017 and 176 showed signs of leafdamagetypicalofinsectherbivory(ColeyampBarone1996)inun-loggedandloggedforestsrespectively Intheexperimentalandpairedcontrolplotsthepercentageofseedlingswithsignsofleafdamage fromherbivorywas similarly small (061and065 inunloggedand logged forest respectively)Thusobservedseed-lingherbivoryrateswerelowAlonger-termstudymayrevealal-teredseedlingherbivoryrateswithlogging(Darrigoetal2018)particularly because herbivorous insect biomass was found toincrease with logging (Ewers etal 2015) Our study examinestheeffectsofintensiveselectiveloggingontheseed-to-seedlingtransitionphaseofacanopydipterocarpHoweverour findingsmaynot represent the fateofseedlingsovera longer timespanbecause ecological changes caused by logging (eg herbivory)could continue to impact the survival of seedlings beyond theseed-to-seedlingtransitionbottleneck(Caughlinetal2015)
F IGURE 4emspTheoddsofpredationofD lanceolataseedsbyvertebratesrelativetonon-vertebratesin(a)naturalplotsand(b)experimental(vertebrateexclosures)andpairedcontrolplotsinunloggedandloggedforestErrorbarsrepresent95confidenceintervals
(a) (b)
F IGURE 5emspTherelationshipsbetweenD lanceolataseedgermination(toppanel)seedlingsurvival(bottompanel)and(af)conspecificseedseedlingdensity(bg)distancefromtheparenttree(ch)seedfall(di)treesizeand(ej)canopycoverinunloggedandloggedforests
(a) (b) (c) (d) (e)
(f) (g) (h) (i) (j)
8240emsp |emsp emspensp PILLAY et AL
WedidnotmanipulatedensityanddistanceindependentlyOuruseof seeddensity gradientsnaturally generatedby thedistancegradient can identify density-dependent patterns of seedling re-cruitment (Harms etal 2000Webbamp Peart 1999)However intheabsenceofexperimentalmanipulationofdensityanddistanceeffects independent of each other our ability to understand thecauses underlying observed patterns of density-dependence inunloggedand logged forests is limited (SwamyampTerborgh2010)Futurestudiesshouldleveragemanipulativeexperimentsforanu-ancedunderstandingof the causes underlying alteredpatterns ofseedling recruitment in the face of anthropogenic disturbances(FreckletonampLewis2006)
5emsp |emspCONCLUSION
We found that for Dryobalanops lanceolata a dipterocarp spe-ciesendangeredby thecommercial timber trade (Ashton1998)multiple stages of seedling recruitment were altered in selec-tively logged forest compared with unlogged forest during amast-fruiting year Future studies should leverage broader log-ging gradients additional species and experimental approachesover longer time frames (Bagchietal2011Martinetal2015Riuttaetal2018Struebigetal2013SwamyampTerborgh2010)to quantify the thresholds of logging intensity abovewhich theecologicalprocessofseedlingrecruitmentmayunravelWehigh-lighttheimportanceofunderstandingtheimpactsofdisturbancessuch as logging on ecological processeswhich can complementnumericalassessmentsofbiodiversitytounmaskimpactsthatmayotherwiseremainhidden
ACKNOWLEDG MENTS
We thank Yayasan Sabah BentaWawasan Sdn Bhd the SabahBiodiversity Council the Sabah Forestry Department theMaliauBasin Management Committee the State Secretary Sabah ChiefMinisterrsquosDepartmenttheMalaysianEconomicPlanningUnitandtheRoyalSocietySouthEastAsiaRainforestResearchPartnershipfor granting permits Our fieldwork was funded by grants fromthe Rufford Small Grants Foundation IDEAWild the Institute ofFoodandAgriculturalSciencesandtheTropicalConservationandDevelopmentProgramattheUniversityofFloridaWethankRyanGray andMinSheng Khoo for coordinating field logistics MainusTausong JeffryAminMohdYusufDidin (Roy)RismanAjangandMelvin Teronggoh for assistance during fieldwork Magat JaparandJeffryAminfor identifyingtreesseedsandseedlingsJeffreyHostetler forhelpwith survival analysis andEmilioBrunaTrevorCaughlin David Newbery and one anonymous reviewer for con-structivecommentsthatgreatlyimprovedthemanuscript
CONFLIC T OF INTERE S T
Nonedeclared
AUTHOR CONTRIBUTIONS
RPconceivedthisstudyRPandRJFraisedthegrantsforfieldworkRPBALRJFandHBdesignedthemethodologyRPcollectedthedataandperformedallstatisticalanalysesRPandFHledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandprovidedfinalapprovalforpublication
DATA ACCE SSIBILIT Y
DatacanbeaccessedthroughtheDryadDigitalRepositoryhttpsdoiorg105061dryaddk4t694 (Pillay Hua Loiselle Bernard ampFletcher2018)
ORCID
Rajeev Pillay httporcidorg0000-0002-7116-6855
R E FE R E N C E S
AshtonP (1998)Dryobalanops lanceolatahttpwwwiucnredlistorgdetails331640(accessed11March2015)
Asner G P Rudel T K Aide T M Defries R amp Emerson R(2009) A contemporary assessment of change in humid trop-ical forests Conservation Biology 23 1386ndash1395 httpsdoiorg101111j1523-1739200901333x
BagchiRGalleryREGripenbergSGurrSJNarayanLAddisCEhellipLewisOT(2014)Pathogensandinsectherbivoresdriverain-forestplantdiversityandcompositionNature50685ndash88httpsdoiorg101038nature12911
Bagchi R Philipson C D Slade E M Hector A Phillips SVillanueva J F hellip Press M C (2011) Impacts of logging ondensity-dependentpredationofdipterocarpseedsinaSouthEastAsian rainforestPhilosophical Transactions of the Royal Society B Biological Sciences 366 3246ndash3255 httpsdoiorg101098rstb20110034
Bartoń K (2016) MuMIn Multi-model inference R package version 1156
BatesDMaumlchlerMBolkerBMampWalkerSC(2015)Fittinglinearmixed-effectsmodelsusing lme4Journal of Statistical Software67httpsdoiorg1018637jssv067i01
BlundellAGampPeartDR(2004)Density-dependentpopulationdy-namicsofadominantrainforestcanopytreeEcology85704ndash715httpsdoiorg10189001-4101
BornJBagchiRBurslemDNilusRTellenbachCPluessARampGhazoulJ(2015)DifferentialresponsesofdipterocarpseedlingstosoilmoistureandmicrotopographyBiotropica4749ndash58httpsdoiorg101111btp12180
BrunaEM (1999) Seedgermination in rainforest fragmentsNature402139httpsdoiorg10103845963
BurnhamKPampAndersonDR(2002)Model Selection and Multimodel Inference A Practical Information-Theoretic ApproachNewYorkNYSpringer-Verlaghttpsdoiorg101007b97636
Caughlin T T Ferguson J M Lichstein J W Zuidema P ABunyavejchewinSampLeveyD J (2015)Lossofanimal seeddis-persalincreasesextinctionriskinatropicaltreespeciesduetoper-vasivenegativedensitydependenceacross life stagesProceedings of the Royal Society B Biological Sciences28220142095httpsdoiorg101098rspb20142095
ChambersJCampMacMahonJA (1994)Adayinthe lifeofaseedMovementsandfatesofseedsandtheirimplicationsfornaturaland
emspensp emsp | emsp8241PILLAY et AL
managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
8234emsp |emsp emspensp PILLAY et AL
E andF in the logged forest andwere able to locate only sevenadultD lanceolatatreesinactivefruitingcondition(withinBlockEtwotreeswithinandaroundBlockFfivetrees)OneofthetreesinBlockEwaslt40mfromtheotherreproductiveconspecificWeremovedthis individual fromthisstudytoensurenon-overlappingseedshadowssincepriorworkonD lanceolatainSarawakBorneo(Itohetal1997)indicatesthatallseedsaredispersedlt40mfromthe parent treeWe included the remaining six individuals in thisstudyThusthesparsenumberofadultconspecificsinactivefruit-ingconditiondictatedoursamplesizeatthelevelofindividualtreesIn the unlogged forest sitewe surveyed approximately 65kmofforesttrailseachinBlocksOG1andOG2andlocated15ndash20(OG1)and20ndash25(OG2)adultD lanceolatatreesinactivefruitingcondition(weexcludedOG3fromthisstudydueto its logginghistory)TheseedshadowsofalltreesinOG1overlappedwiththoseofatleastoneotherconspecificadultThereforeweselectedsevenindividu-alsinOG2whoseseedshadowsdidnotoverlapwiththoseofotherreproductiveconspecificsWeconsideredeachindividualfocaltreeasanexperimentalunitresultinginsevenandsixreplicatesatthelevelofindividualtreesinunloggedandloggedforestrespectivelyIndividualtreesareoftenusedasexperimentalunitsinseeddisper-salandseedlingrecruitmentstudiesandmaybeconsidered inde-pendentsamplesiftheirseedshadowsdonotoverlapwiththoseofotherconspecifics (Bagchietal2011HolbrookampLoiselle2009Poulsenetal2012)
Thesevenfocaltreesinunloggedforestwere303mapartonaveragewith the smallest pairwise distance between two treesbeing40mThesixfocaltreesinloggedforestwere1690mapartonaveragewiththesmallestpairwisedistancebetweentwotreesbeing244mandcoverconsiderable landscapeheterogeneity interms of logging intensity and time since logging (Wearn etal2013)Onaverageourfocaltreeswerearound56timesfurtherapart from each other in logged forest than in unlogged forestwhichpotentiallyindicatestheintensityofextractionifD lance-olatapopulationdensitiesweresimilar inbothforesttypespriortologging
Wesetupfour32mtransectsextendingfromthebaseofeachfocaltreewiththefirsttransectorientedalongarandomcompassdirection and each subsequent transect at 90deg from the previous(Figure2)We constrained transect length to 32m because priorwork indicated that few seeds reached this distance (Itoh etal1997)AlongeachtransectweusedseedtrapstoquantifytheseedcropandseeddispersaldistancesettingthemupsoonafterseedfallcommencedinearlyAugust2014Wedeployedtheseedtrapsonalog2scaleat124816and32mdistances(n=24seedtrapstreeFigure2)Eachtrapwasa1times1mnylonmeshnetsuspendedby1-mtallPVCpipesateachcornerThevalidityofourdatareliesontheassumptionthatourfocaltreeshadnon-overlappingseedshadowsSince995of all seeds fell into the seed trapswithin16m fromtheirrespectiveparenttrees(seeSection3)adistancethat is lessthanhalfoftheminimumdistancebetweenanyofourfocal trees(ie40m)theseedsweincludedinthisstudyshouldbepredomi-nantlyifnotentirelyfromtheirrespectiveparenttrees
Wemonitoredseedpredationanddensity-dependentpatternsofgerminationandseedlingsurvivalof individualseedsthatnatu-rally dispersed into individual 1times1m unmanipulated monitoringplots (hereafter ldquonatural plotsrdquo) We thus utilized the conspecificseedseedlingdensitygradientnaturallygeneratedbythedistancegradient forourassessmentofNDDWeplacednaturalplots2mtotheleftoftheseedtrapsalongeachtransectat24816and32m distances (n=20 natural plotstree Figure2) Additionallyaround 1month after the commencement of seedfall we set upvertebrate-exclosure plots (hereafter ldquoexperimental plotsrdquo) andpairednon-exclosureplots(hereafterldquocontrolplotsrdquo)totestfortherelativecontributionofvertebratesversusinsectsandfungitoseedpredationWeplacedexperimentalandcontrolplotsat2and32mdistancesalongone randomlyselected transectateach focal tree(n=2 plot pairstree Figure2)At 32mweplaced eachplot pair2mfromeachotherandontherightsideofthecorrespondingseedtraprandomlyassigningtherelativepositionofexperimentalversuscontrolplots(iewhichplotwasplacedadjacenttothecorrespond-ingseedtrap)At2mduetolimitedspacenearthebaseofthefocaltreeweplacedoneplotontherightofthecorrespondingseedtrapandthepairedplotatthecorrespondingpositionalongthediago-nallyoppositetransectrandomlyassigningtherelativepositionofexperimentalversuscontrolplots (Figure2)Dueto logisticalcon-straintsweomittedoneof themost remote focal trees in loggedforestinthiscomparisonandinsteadsetuptwoadditionalplotpairsinthesamewayaroundanotherofourfocaltreeswhichwasmore
F IGURE 2emspStudydesignshowingseedtraps(at124816and32mdistances)naturalplots(at24816and32mdistances)andpairedexperimental(vertebrateexclosures)andcontrolplots(at2and32mdistances)alongfour-32mtransectsfromthebaseoffocalD lanceolatatreesSeedtrapsnaturalandcontrolplotswere1times1minareaExperimentalplotswere1times1times05mFigurenottoscale
12 4 8 16 32
Focal treeSeed trapNatural plotExperimental plotControl plot
emspensp emsp | emsp8235PILLAY et AL
accessible Experimental plotswere 1times1times05mwith the exclo-suremade fromsteelwireof127times127cmmeshsize toexcludeallvertebrateseedpredatorsbutnotinsectseedpredatorsorfungalpathogens(Figure1)Controlplotswereopentoallseedpredatorsandpathogens
ForthepairedexperimentalandcontrolplotsweaddedD lance-olataseedsatpredefineddensities~1monthaftercommencementof seedfall and thereafter continuously removed all conspecificseedsthatfellintothecontrolplotsthroughoutthedurationofthestudyWeused a seeddensity of 5seedsm2 for thepairedplotsat2mdistancesand50seedsm2 forthoseat32mdistancesForseeding the plots we collected intact (ie no visible evidence ofpredatorattack)matureseedsfromaround20non-focalD lanceo-latatreesinunloggedforestWethoroughlymixedtheseseedsandplacedthemonthesoilsurfaceinaregulargridtomimicthenaturalseedfallpatterninwhichseedsgyratefromtheparenttreesandlandonthegroundWethusdistributed770seeds(n=28experimentalandpairedcontrolplots)ineachforesttypeWenotethatthispartofthestudyaimstoprovideonlyasupportingassessmentoftherel-ative importanceofvertebrateandnon-vertebrateseedpredatorsinunloggedandloggedforestsWedidnotattempttomanipulatedensity anddistance independentlydue to logisticaldifficulties incollecting and sowing additional seeds a time-sensitive undertak-ingbecauseoftherapidityatwhichseedsgerminatetogenerateaspectrumofseeddensities thatwouldreflectscenariosunderun-loggedandloggedconditions(cfBagchietal2011Poulsenetal2012)
24emsp|emspData collection
We collected seeds from the traps at two census intervals be-tween12Augustand4Novemberinloggedforestandbetween1Septemberand22October inunloggedforestWemonitoredthefateofeveryseeduponinitiatingthenaturalplots(atthesameinter-valsastheseedtraps)untiltheendofthestudyWetaggedallseedswithnumberedplastictagsstapledtotheirwings(Figure1)andcon-tinuedtaggingseedsthatnewlyfell intothenaturalplotsAteachcensusintervalwerecordedthenumberofseedsthatsurvivedanddiedineachplotForsurvivingseedswerecordediftheywereger-minatingandsubsequentlywhether they recruited into seedlingsWealsoscoredeachseedintooneofthefollowingcategories(afterBagchietal2011)intact(novisiblesignsoffungalinsectorverte-brateattack)germinated(definedasemergenceoftheradicleItohetal1995)seedling(ge5cmtallexpandedtrueleaves)vertebratedepredated(partiallyeatengnawedorremoved)insectdepredated(withentryexitholes) fungusdepredated(withfungalsporesmy-celia)Wenote that the seeds falling into the natural plotswouldlikely be exposed to both pre-dispersal and postdispersal insectpredators(Bagchietal2011)Wewerecarefultoclassifydepreda-tionstatusonthebasisofthepredatorthatweinitiallyrecordedtohaveattackedtheseedseedling(LewisampGripenberg2008)Thusaseedwithinsectentryexitholesattheinitialcensusthatwassub-sequentlypartiallyeatenorremovedbyvertebrateswasscoredas
predatedbyinsectsDuetothedifficultyinascertainingtheinitialpredatorbetweeninsectsandfungalpathogenswecollapsedthemintothenon-vertebratecategoryWethususedtwopredatorcat-egoriesvertebrateversusnon-vertebrate
WemeasuredasetofecologicalcovariatesthatcanpotentiallyinfluencevariousstagesofseedlingrecruitmentandthusshouldbeaccountedforinexaminingtheimpactsofloggingThesecovariatesincludedthreemeasuresoftreesizethataredeterminantsofseedcropsizeanddispersaldistanceDBHheightandcrowndiameter(CousensDythamampLaw2008NorghauerNockampGrogan2011)We also measured percentage canopy cover as a proxy for lightavailabilitywhich in turnmay influencegerminationand seedlingsurvival(Kobe1999)SeeSupportinginformationAppendixS1fordetailsonthesemeasurements
25emsp|emspStatistical analyses
Wefirstusedprincipal-componentsanalysis(PCA)toidentifymajortrends intreesizedataandreducethenumberofvariablesrepre-sentingtreesizeThefirstprincipalcomponent(PC1)waspositivelycorrelatedwithallthreevariablesrepresentingtreesizehadanei-genvaluegt1andexplained764ofthetotalvarianceintreesizedata (Supporting information Table S1) We used the componentscoresgeneratedfromthe loadingsofPC1asasurrogatefor treesizeinfurtherstatisticalanalyses
Wethenusedgeneralizedlinearmixedmodels(GLMMs)toana-lyzetheimpactsofloggingonseedcropsizeanddispersalpatternsusingthenumberofseeds ineachseedtrapastheresponsevari-ableWeusedforesttype(unloggedvslogged)distancefromthefocaltreePC1(hereafterldquotreesizerdquo)andalltwo-wayinteractionsbetween forest type and the other variables as fixed effectsWeincluded individualseedtrapsnestedwithintreesasa random in-terceptinallmodelsWeassumedaPoissonerrordistributionandaloglinkfunctionWetestedforoverdispersionbycalculatingthesumofsquaredPearsonresidualsandcomparing it totheresidualdegreesoffreedomforeachmodel(ZuurIenoWalkerSavelievampSmith2009)
WealsousedGLMMstoanalyzetheimpactofloggingontherelative role of vertebrates versus non-vertebrates inD lanceo-lataseedandseedlingpredationOurobservationsindicatedthatmostseedlingsdiedfrompredation(eguprootedandpartiallycompletelyconsumedremovedbyvertebratescotyledonsofger-minatedseedlingsdestroyedbyinsectsandorfungalpathogens)rather than from leaf damage typically inflicted by herbivores(ColeyampBarone1996)Thereforewepooleddataon seedandseedling predation For the natural plotswe scored each seedseedling as depredated by either vertebrate or non-vertebratepredators and then modeled the probability of a seedseedlingbeingdepredatedbyvertebrates (relative tonon-vertebrates)asa functionof forest typeas the fixedeffectvariableForpairedexperimental and controlplotswecounted thenumberofdep-redated seedsseedlings out of the total number of seeds andthenmodeledtheprobabilityofseedseedlingpredationWeused
8236emsp |emsp emspensp PILLAY et AL
foresttypeandtreatmenttype(experimentalvscontrolplots)asfixedeffectvariablesInbothanalysesofseedseedlingpredationweincludedindividualplotssequentiallynestedwithintransectsandtreesasarandominterceptWeassumedabinomialerrordis-tribution and a logit link functionWe note that nomadic herdsof bearded pigs destroyed our experimental exclosures for fourout of seven trees in unlogged forest (but not in logged forest)between1and19October(~30daysfromtheonsetofseedseed-lingmonitoringintheseplots)Thereforeforunloggedforestweonly considered data from the paired experimental and controlplotsforthethreetreesthatwerenotdepredatedbybeardedpigs(n=330seeds12plots)
WeusedCoxregressionmixed-effectssurvivalmodelstoan-alyzethe impactof loggingongerminationandseedlingsurvivalatthelevelofindividualseedsandseedlingswithdatacollectedfromthenaturalplotsWefirstmodeledseedsurvivaluntilger-minationwithsurvivalmodeledasdailygerminationrateOftheseeds that germinatedwe subsequentlymodeled daily seedlingsurvivaluntil3monthsafterseedfallWeincorporatedseedseed-lingageandusedright-censoring ifaseedseedlingsurvivedbe-yondtheendofthemonitoringperiodForfixedeffectvariablesweincludedforesttypelocal-scale(1m2)conspecificseedseed-lingdensity (hereafter ldquoconspecificseeddensityrdquo)distancefromthe parent tree and percentage canopy coverWe also includedtree size and total conspecific seedfall at each tree during thestudy (surrogate formedium-scale seed density) as fixed effectvariables because these factorsmay vary between the two for-esttypesandpotentiallyinfluenceseedlingrecruitmentpatterns(Bagchi etal 2011 CurranampWebb 2000) Lastlywe includedinteractions between forest type and the five latter variablesForrandomeffectswesequentiallynestedtheidentitiesofplotswithintransectsandtreestocontrolforpotentialvariationinmi-crotopographythatcouldcausedifferentialgerminationandseed-lingsurvival(Bornetal2015)
Fortheanalysesdescribedabovewebuiltsetsofsub-modelsbasedontheglobalmodelandcomparedmodelsusingAkaikersquos
Information Criterion adjusted for sample size (AICc) (BurnhamampAnderson2002)WeconsideredmodelsfromthelowestAICc until thecumulativemodelweightexceeded95Wethenusedthis95confidencemodelsetasthebasisformodelaveragingandstatisticalinference(BurnhamampAnderson2002)Weconductedall statistical analyses inR (v 321) (RDevelopmentCoreTeam2017)andusedtheglmer function in thepackageldquolme4rdquo (BatesMaumlchler Bolker ampWalker 2015) to fit all GLMMs the packageldquocoxmerdquo(Therneau2015)tofitsurvivalmodelsandthepackageldquoMuMInrdquo(Bartoń2016)formodelselectionandaveraging
3emsp |emspRESULTS
31emsp|emspImpact of logging on seed crop size
ThefivemostparsimoniousmodelswithacumulativeAICcweightof100(Supporting informationTableS2) indicatedthat foresttypedistancefromthefocaltreetreesizeandinteractionsbe-tweenforesttypeandtheothervariableshadsupportinexplain-ingvariationinD lanceolataseedcropsizeanddispersalpatternsConsistentwithprediction1theseedcroptendedtobesmallerin logged forest than in unlogged forest evenwhen accountingfor tree size (Figure3a Table1a)Over ~3months (85days)wecollected2105(n=168traps)and718(n=144traps)seedsinun-loggedandloggedforestrespectivelyTheaverageseeddensity(plusmn1SE) inunloggedforestwas1252(plusmn099)seedsm2comparedwith498(plusmn048)seedsm2inloggedforestThenumberofseedsdeclinedwithincreasingdistancefromthefocaltreesinbothfor-est types (Figure3bTable1a)Consistentwithpatternsof localseed dispersal (Itoh etal 1997) only 06of all trapped seedslanded at 32m in unlogged forest and none in logged forestLarger trees tended toproducemoreseeds inboth forest types(Figure3cTable1a)althoughtreesinloggedforestweresmallerthanthoseinunloggedforest(SupportinginformationFigureS1)Wefoundnoevidenceforoverdispersion(SupportinginformationTableS3)
F IGURE 3emspTherelationshipbetweenD lanceolataseeddensityand(a)foresttype(b)distancefromfocaltreesineachforesttypeand(c)treesizeineachforesttypeErrorbarsandtheshadedregionsofthecurvesarethepredicted95confidenceintervals
(a) (b) (c)
emspensp emsp | emsp8237PILLAY et AL
32emsp|emspImpact of logging on the predation of seeds and seedlings
Over3monthswerecordedanoverallseedandseedlingpredationrate of 866 and 836 in unlogged (n=1423 seeds 140 naturalplots)andlogged(n=646seeds120naturalplots)forestrespec-tivelyAsmallnumberofseeds(unloggedforest5loggedforest8)diedofdesiccationConsistentwithprediction2therewasashiftinthefunctionalroleofseedpredatorsawayfromnon-vertebratesto-wardvertebratesinloggedforest(Figure4ab)Inthenaturalplotsthe log odds of a seedseedling being depredated by vertebrates(relativetonon-vertebrates)werehigherinloggedforestthaninun-loggedforest(βlogged079SE05095CIminus028to185Figure4aSupportinginformationTableS4)Furthersupportingprediction2the logoddsofseedandseedlingpredationwere lower intheex-perimentalexclosureplotsthaninthecontrolplotsinloggedforest(βlogged-exclosureminus210SE05795CIminus343 tominus097Figure4b)In contrast the effect of exclosure treatments on seed predationtendedtobeweakerinunloggedforest(βunlogged-exclosureminus102SE 08895CIminus290to089Figure4bSupportinginformationTableS5)
33emsp|emspImpact of logging on density- dependent germination and seedling survival
We monitored the germination and survival status of seeds thatwerealiveinthenaturalplotsatthefirstcensus(603and227seedsin unlogged and logged forest respectively) until the end of thestudy The sixmost parsimoniousmodelswith a cumulativeAICcweightof97(SupportinginformationTableS6)indicatedthatfor-est type conspecific seed density distance from the parent treeseedfall tree size canopy cover and interactions between foresttypeandtheothervariableshadsupport inexplainingvariation inseedgerminationSeedsfacedgreaterhazard(iehigherprobabilityofmortality) inloggedforestthaninunloggedforest(Table1b)as471ofseedsfailedtogerminateinloggedforestcomparedwith08 in unlogged forestHigher conspecific seed densitywas as-sociatedwithlowerseedmortalityinunloggedforestandthisrela-tionshipalsotendedtoapplyinloggedforest(Figure5aTable1b)With increasingdistancefromparenttreesseedmortalitytendedto increase in both forest types but this relationshipwasweakerin logged forest (Figure5b Table1b) Higher seedfall and largertreesizetendedtobeassociatedwithlowerseedmortalityinbothforest types (Figure5cdTable1b)With increasing canopy coverseedmortality tended to increase inboth forest types (Figure5eTable1b)
Forexplainingvariationinseedlingsurvivalthetwomostparsi-moniousmodelswithacumulativeAICcweightof99(SupportinginformationTableS7) indicated that forest type conspecific seeddensity distance from the parent tree seedfall tree size canopycoverandinteractionsbetweenforesttypeandtheothervariableshad support Of the seeds that germinated seedlings tended tohavelowerprobabilityofmortalityinloggedforestthaninunlogged
forest(Table1c)as817ofgerminatedseedlingssurviveduptotheendofthestudyinloggedforestcomparedwith311inunloggedforestHigherconspecificseedlingdensitytendedtobeassociatedwithhigherseedlingmortality inunloggedforestbut inconsistentwith prediction 3 this relationship was reversed in logged forest(Figure5f Table1c) With increasing distance from parent treesseedlingmortalityincreasedinunloggedforestbutthisrelationshiptendedtobereversedinloggedforest(Figure5gTable1c)Higherseedfall tended tobe associatedwithhigher seedlingmortality inunloggedforestbutthisrelationshipalsotendedtobereversedinloggedforest(Figure5hTable1c)Likegerminationlargertreesizetendedtobeassociatedwithlowerseedlingmortalityinbothforesttypesandthisrelationshipwasstrongerinloggedforest(Figure5iTable1c)With increasingcanopycoverseedlingmortalitytendedtoincreaseinunloggedforestbutthisrelationshiptendedtobere-versedinloggedforest(Figure5jTable1c)
4emsp |emspDISCUSSION
Ourresultsdemonstratehowmultiplestagesoftheseedlingrecruit-mentprocessofacanopytreespeciesmaybealteredwhentropicalforestsaredegradedbyintensiveldquoselectiverdquologgingConsistentwithourpredictions the remaining reproductive trees in logged forestproducedamarkedlysmallerseedcropthanthetreesinunloggedforestevenafteraccountingfortreesizeandthefunctionalroleofvertebratesinseedpredationincreasedinloggedforestwhilethatof non-vertebrates declined The strength of density-dependencein dipterocarpsmay change frompositive to negative at differentlife stages (Blundell amp Peart 2004 Curran ampWebb 2000) Thisappearedtobethecase inunloggedforestwheregermination in-creasedwithlocal-scaleconspecificseeddensitypossiblybecausepredatorsweresatiatedbythehighmast-fruitingseeddensitiesbutseedlingsurvivaltendedtodecline(Figure5afTable1bc)HoweverinconsistentwithourpredictionofstrongerNDDinloggedforestgermination and especially seedling survival increasedwith local-scaleconspecificseeddensitywhichsuggeststhatloggingmayhaveaffectedpredator-mediatedNDDduringtheseed-to-seedlingtran-sitionbottleneck inD lanceolata Importantlyourfindingsappliedtoamast-fruitingyearwhenmostdipterocarprecruitmentoccurs(CurranampLeighton2000Janzen1974)suggestingthat intensiveloggingmaypotentiallyaffectlong-termpopulationdynamicsofD lanceolataOur findings add to knowledge of how ecological pro-cesses responsible for themaintenanceofbiodiversitymaybeaf-fectedbylogging(DarrigodosSantosampVenticinque2018Ewersetal2015Schleuningetal2011Woodcocketal2013)
Increasing edaphic and drought stress in reproducing treesin logged forest may have contributed to the reduced seed crop(Curran etal 1999 Hardwick etal 2015) The consequences ofseed limitation in logged forests for sapling and ultimately adulttree recruitment remain largelyunexploredbutmaybedetrimen-tal for long-term tree population dynamics (Caughlin etal 2015)Changes in the functional roles of non-vertebrate seed predators
8238emsp |emsp emspensp PILLAY et AL
relativetovertebratesinloggedforestmaybedrivenbynumericalchanges inpredatorabundanceacrossgroups (Ewersetal2015)The altered microclimatic conditions in logged forests are likelyhostile to populations of insect seed predators and fungal patho-gens(Ewersetal2015Hardwicketal2015)Converselylogged
forestsmayprovideincreasedresourceavailabilityforrodentseedpredatorsandthusbenefittheirpopulations(Ewersetal2015)
Theuniqueecologyofmast-fruitingandtheimpactthisphenom-enonmayhavesustainedinloggedforestmayexplainthecomplexdensity-dependent patterns of germination and seedling survival(Figure5af)On theonehand in unlogged forest predator satia-tionmayhavebeenoccurringatthehighseeddensitiesduringthemast(Janzen1970)aspotentiallysupportedbyourfindingthatger-minationtendedtoincreasewithhigherseedfall(Figure5cBagchietal2011CurranampWebb2000)Indeedmast-fruitinghasbeenhypothesizedtobeanevolutionaryresponsetodensity-dependentmortality factors allowing seeds to escape predation by satiatingseedpredators (Janzen19701974)Ontheotherhand in loggedforesttheconcentratedseeddensitiesunderspatiallyisolatedadulttreesmayallowNDDtooperate(Bagchietal2011CurranampWebb2000)Howeverourfindingsofincreasedgerminationandespeciallyseedlingsurvivalwithhigherconspecificseeddensityinloggedfor-est(Figure5afTable1bc)werecontrarytotheexpectationsunderNDDandmaybeassociatedwiththediminishedfunctionalroleofnon-vertebrate seedpredators in logged forest (Figure4)NDD isprimarily driven by host-specific insect seed predators and fungalpathogenswhichtendtoconcentrateamongthehigh-seedseedingdensitiesunderthecrownsofparenttreestherebycausinghighermortalitywhere densities are higher (Bagchi etal 2014 Connell1971 Janzen 1970) These non-vertebrate seed predators andpathogensmaybedeclining in logged forests (Ewers etal 2015)andtheirecologicalroleinmaintainingNDDmaybediminishedIncontrastthetendencyofvertebratestoforageoverlargeareasmayrender predation-relatedmortality to bemore spatially heteroge-neousrelativetoseedseedlingdensities(SwamyampTerborgh2010)
Wenotethatseedcropsizegerminationandseedlingsurvivaltendedtoincreaseforlargertreesinbothforesttypes(Figures3c5di)Thissuggeststhatselectiveloggingpracticesthatharvesttim-ber at sustainable rates and followsilviculturalpracticesdesignedtominimizedamagetotheresidualstand(Asneretal2009Martinetal2015Putzetal2012)arecriticaltopreventseedlingrecruit-mentfailure indipterocarpforestsSeedgerminationandseedlingsurvivalofD lanceolatatendstobepositivelyassociatedwithlightavailability (Itoh etal 1995) which likely explains why seed andseedling mortality tended to increase with higher canopy cover(Figure5ej)
41emsp|emspCaveats and limitations
OurstudyincludedsevenandsixD lanceolatatreesasindepend-ent experimental units in unlogged and logged forests respec-tively (cfBagchietal2011HolbrookampLoiselle2009Poulsenetal 2012) The spatially clumped distributions of most adultfruiting individuals inunlogged forestand the fewspatially scat-teredadultdipterocarpsremaininginloggedforest(ofallspeciesD lanceolata was the most abundant at seven individuals) pre-cludedadditionalreplicationatthelevelofindividualtreeswithinforesttypeThesparsenumberofadultdipterocarpsinthelogged
TABLE 1emspModelaveragedestimatesexplainingvariationin(a)seedcropsize(b)germinationand(c)seedlingsurvival(upto3monthsafterseedfall)ofD lanceolatainrelationtothepredictorvariablesthatweresupportedbyAICc-basedmodelselectioncriteria(SupportinginformationTablesS2S6S7)
Response and predictor variables Estimate (SE) 95 CI
(a)Seedcropsize
Intercept 300(029) 240ndash352
Loggedforest minus080(048) minus172ndash007
Distance minus013 (001) minus014tominus011
Loggedforesttimesdistance minus001(001) minus005ndash001
Treesize 006(014) minus018ndash060
Loggedforesttimestreesize 001(010) minus054ndash080
(b)Germination
Logged forest 468 (362) 269ndash1096
Conspecific seed density minus271 (238) minus744tominus075
Logged foresttimesconspecific seed density
265 (235) 105ndash723
Distance 003(018) minus062ndash133
Loggedforesttimesdistance minus002(016) minus134ndash091
Seedfall minus084(157) minus602ndash104
Loggedforesttimesseedfall 024(149) minus422ndash1428
Treesize minus018(098) minus639ndash329
Loggedforesttimestreesize minus014(108) minus1072ndash474
Canopycover 001(032) minus217ndash255
Loggedforesttimescanopycover 015(084) minus155ndash775
(c)Seedlingsurvival
Loggedforest minus710(403) minus1500ndash081
Conspecificseedlingdensity 030(015) minus001ndash060
Logged foresttimesconspecific seedling density
minus170 (043) minus255tominus086
Distance 015 (009) 002ndash032
Logged foresttimesdistance minus104 (067) minus231 tominus012
Seedfall 003(058) minus119ndash126
Loggedforesttimesseedfall minus203(307) minus863ndash389
Treesize minus003(096) minus206ndash199
Logged foresttimestree size minus316 (205) minus706 tominus033
Canopycover 027(028) minus024ndash087
Loggedforesttimescanopycover minus034(110) minus271to191
NotesResultsforseedcropsizerepresentcoefficients(log-scale)esti-matedwithgeneralizedlinearmixedmodelsResultsforgerminationandseedling survival represent loghazardsestimatedwithCox regressionmixed-effectssurvivalmodelsEstimatesinitalicsindicatethatthe95confidenceintervalsdidnotoverlapzerosuggestingastrongeffectofthepredictorvariableonthecorrespondingresponsevariable
emspensp emsp | emsp8239PILLAY et AL
forestisareflectionofthepopulationreductionmanytimbertreespeciesaresubjected toafter intensiveselective logging (Martinetal2015)
The variable density of adultD lanceolata trees between un-logged and logged forests may introduce confounding negativedensity-dependentneighbourhoodeffectsonseedlingrecruitment(BlundellampPeart2004StollampNewbery2005)PreviousresearchontheDipterocarpaceaesuggeststhatneighbourhoodeffectsmayoccurwhenconspecificadultsarewithin20mofeachother(StollampNewbery2005)Ourrequirementofnon-overlappingseedshad-owsbetweenfocaltreesensuredthattreeswereseparatedbyatleast40mTherelativelylargerdistancebetweenthefocaltreesinourstudycomparedwiththethresholddistanceof20matwhichneighbourhoodeffectsmayoccur(StollampNewbery2005)shouldthusservetominimizethispotentialconfoundingfactor
Inanalyzingagentsofseedandseedlingpredationwedidnotdistinguishbetweenthedifferentprocessesofseedlingpredation
andherbivoryOftheseedlingsthatwerealiveinthenaturalplotsat the end of the study 017 and 176 showed signs of leafdamagetypicalofinsectherbivory(ColeyampBarone1996)inun-loggedandloggedforestsrespectively Intheexperimentalandpairedcontrolplotsthepercentageofseedlingswithsignsofleafdamage fromherbivorywas similarly small (061and065 inunloggedand logged forest respectively)Thusobservedseed-lingherbivoryrateswerelowAlonger-termstudymayrevealal-teredseedlingherbivoryrateswithlogging(Darrigoetal2018)particularly because herbivorous insect biomass was found toincrease with logging (Ewers etal 2015) Our study examinestheeffectsofintensiveselectiveloggingontheseed-to-seedlingtransitionphaseofacanopydipterocarpHoweverour findingsmaynot represent the fateofseedlingsovera longer timespanbecause ecological changes caused by logging (eg herbivory)could continue to impact the survival of seedlings beyond theseed-to-seedlingtransitionbottleneck(Caughlinetal2015)
F IGURE 4emspTheoddsofpredationofD lanceolataseedsbyvertebratesrelativetonon-vertebratesin(a)naturalplotsand(b)experimental(vertebrateexclosures)andpairedcontrolplotsinunloggedandloggedforestErrorbarsrepresent95confidenceintervals
(a) (b)
F IGURE 5emspTherelationshipsbetweenD lanceolataseedgermination(toppanel)seedlingsurvival(bottompanel)and(af)conspecificseedseedlingdensity(bg)distancefromtheparenttree(ch)seedfall(di)treesizeand(ej)canopycoverinunloggedandloggedforests
(a) (b) (c) (d) (e)
(f) (g) (h) (i) (j)
8240emsp |emsp emspensp PILLAY et AL
WedidnotmanipulatedensityanddistanceindependentlyOuruseof seeddensity gradientsnaturally generatedby thedistancegradient can identify density-dependent patterns of seedling re-cruitment (Harms etal 2000Webbamp Peart 1999)However intheabsenceofexperimentalmanipulationofdensityanddistanceeffects independent of each other our ability to understand thecauses underlying observed patterns of density-dependence inunloggedand logged forests is limited (SwamyampTerborgh2010)Futurestudiesshouldleveragemanipulativeexperimentsforanu-ancedunderstandingof the causes underlying alteredpatterns ofseedling recruitment in the face of anthropogenic disturbances(FreckletonampLewis2006)
5emsp |emspCONCLUSION
We found that for Dryobalanops lanceolata a dipterocarp spe-ciesendangeredby thecommercial timber trade (Ashton1998)multiple stages of seedling recruitment were altered in selec-tively logged forest compared with unlogged forest during amast-fruiting year Future studies should leverage broader log-ging gradients additional species and experimental approachesover longer time frames (Bagchietal2011Martinetal2015Riuttaetal2018Struebigetal2013SwamyampTerborgh2010)to quantify the thresholds of logging intensity abovewhich theecologicalprocessofseedlingrecruitmentmayunravelWehigh-lighttheimportanceofunderstandingtheimpactsofdisturbancessuch as logging on ecological processeswhich can complementnumericalassessmentsofbiodiversitytounmaskimpactsthatmayotherwiseremainhidden
ACKNOWLEDG MENTS
We thank Yayasan Sabah BentaWawasan Sdn Bhd the SabahBiodiversity Council the Sabah Forestry Department theMaliauBasin Management Committee the State Secretary Sabah ChiefMinisterrsquosDepartmenttheMalaysianEconomicPlanningUnitandtheRoyalSocietySouthEastAsiaRainforestResearchPartnershipfor granting permits Our fieldwork was funded by grants fromthe Rufford Small Grants Foundation IDEAWild the Institute ofFoodandAgriculturalSciencesandtheTropicalConservationandDevelopmentProgramattheUniversityofFloridaWethankRyanGray andMinSheng Khoo for coordinating field logistics MainusTausong JeffryAminMohdYusufDidin (Roy)RismanAjangandMelvin Teronggoh for assistance during fieldwork Magat JaparandJeffryAminfor identifyingtreesseedsandseedlingsJeffreyHostetler forhelpwith survival analysis andEmilioBrunaTrevorCaughlin David Newbery and one anonymous reviewer for con-structivecommentsthatgreatlyimprovedthemanuscript
CONFLIC T OF INTERE S T
Nonedeclared
AUTHOR CONTRIBUTIONS
RPconceivedthisstudyRPandRJFraisedthegrantsforfieldworkRPBALRJFandHBdesignedthemethodologyRPcollectedthedataandperformedallstatisticalanalysesRPandFHledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandprovidedfinalapprovalforpublication
DATA ACCE SSIBILIT Y
DatacanbeaccessedthroughtheDryadDigitalRepositoryhttpsdoiorg105061dryaddk4t694 (Pillay Hua Loiselle Bernard ampFletcher2018)
ORCID
Rajeev Pillay httporcidorg0000-0002-7116-6855
R E FE R E N C E S
AshtonP (1998)Dryobalanops lanceolatahttpwwwiucnredlistorgdetails331640(accessed11March2015)
Asner G P Rudel T K Aide T M Defries R amp Emerson R(2009) A contemporary assessment of change in humid trop-ical forests Conservation Biology 23 1386ndash1395 httpsdoiorg101111j1523-1739200901333x
BagchiRGalleryREGripenbergSGurrSJNarayanLAddisCEhellipLewisOT(2014)Pathogensandinsectherbivoresdriverain-forestplantdiversityandcompositionNature50685ndash88httpsdoiorg101038nature12911
Bagchi R Philipson C D Slade E M Hector A Phillips SVillanueva J F hellip Press M C (2011) Impacts of logging ondensity-dependentpredationofdipterocarpseedsinaSouthEastAsian rainforestPhilosophical Transactions of the Royal Society B Biological Sciences 366 3246ndash3255 httpsdoiorg101098rstb20110034
Bartoń K (2016) MuMIn Multi-model inference R package version 1156
BatesDMaumlchlerMBolkerBMampWalkerSC(2015)Fittinglinearmixed-effectsmodelsusing lme4Journal of Statistical Software67httpsdoiorg1018637jssv067i01
BlundellAGampPeartDR(2004)Density-dependentpopulationdy-namicsofadominantrainforestcanopytreeEcology85704ndash715httpsdoiorg10189001-4101
BornJBagchiRBurslemDNilusRTellenbachCPluessARampGhazoulJ(2015)DifferentialresponsesofdipterocarpseedlingstosoilmoistureandmicrotopographyBiotropica4749ndash58httpsdoiorg101111btp12180
BrunaEM (1999) Seedgermination in rainforest fragmentsNature402139httpsdoiorg10103845963
BurnhamKPampAndersonDR(2002)Model Selection and Multimodel Inference A Practical Information-Theoretic ApproachNewYorkNYSpringer-Verlaghttpsdoiorg101007b97636
Caughlin T T Ferguson J M Lichstein J W Zuidema P ABunyavejchewinSampLeveyD J (2015)Lossofanimal seeddis-persalincreasesextinctionriskinatropicaltreespeciesduetoper-vasivenegativedensitydependenceacross life stagesProceedings of the Royal Society B Biological Sciences28220142095httpsdoiorg101098rspb20142095
ChambersJCampMacMahonJA (1994)Adayinthe lifeofaseedMovementsandfatesofseedsandtheirimplicationsfornaturaland
emspensp emsp | emsp8241PILLAY et AL
managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
emspensp emsp | emsp8235PILLAY et AL
accessible Experimental plotswere 1times1times05mwith the exclo-suremade fromsteelwireof127times127cmmeshsize toexcludeallvertebrateseedpredatorsbutnotinsectseedpredatorsorfungalpathogens(Figure1)Controlplotswereopentoallseedpredatorsandpathogens
ForthepairedexperimentalandcontrolplotsweaddedD lance-olataseedsatpredefineddensities~1monthaftercommencementof seedfall and thereafter continuously removed all conspecificseedsthatfellintothecontrolplotsthroughoutthedurationofthestudyWeused a seeddensity of 5seedsm2 for thepairedplotsat2mdistancesand50seedsm2 forthoseat32mdistancesForseeding the plots we collected intact (ie no visible evidence ofpredatorattack)matureseedsfromaround20non-focalD lanceo-latatreesinunloggedforestWethoroughlymixedtheseseedsandplacedthemonthesoilsurfaceinaregulargridtomimicthenaturalseedfallpatterninwhichseedsgyratefromtheparenttreesandlandonthegroundWethusdistributed770seeds(n=28experimentalandpairedcontrolplots)ineachforesttypeWenotethatthispartofthestudyaimstoprovideonlyasupportingassessmentoftherel-ative importanceofvertebrateandnon-vertebrateseedpredatorsinunloggedandloggedforestsWedidnotattempttomanipulatedensity anddistance independentlydue to logisticaldifficulties incollecting and sowing additional seeds a time-sensitive undertak-ingbecauseoftherapidityatwhichseedsgerminatetogenerateaspectrumofseeddensities thatwouldreflectscenariosunderun-loggedandloggedconditions(cfBagchietal2011Poulsenetal2012)
24emsp|emspData collection
We collected seeds from the traps at two census intervals be-tween12Augustand4Novemberinloggedforestandbetween1Septemberand22October inunloggedforestWemonitoredthefateofeveryseeduponinitiatingthenaturalplots(atthesameinter-valsastheseedtraps)untiltheendofthestudyWetaggedallseedswithnumberedplastictagsstapledtotheirwings(Figure1)andcon-tinuedtaggingseedsthatnewlyfell intothenaturalplotsAteachcensusintervalwerecordedthenumberofseedsthatsurvivedanddiedineachplotForsurvivingseedswerecordediftheywereger-minatingandsubsequentlywhether they recruited into seedlingsWealsoscoredeachseedintooneofthefollowingcategories(afterBagchietal2011)intact(novisiblesignsoffungalinsectorverte-brateattack)germinated(definedasemergenceoftheradicleItohetal1995)seedling(ge5cmtallexpandedtrueleaves)vertebratedepredated(partiallyeatengnawedorremoved)insectdepredated(withentryexitholes) fungusdepredated(withfungalsporesmy-celia)Wenote that the seeds falling into the natural plotswouldlikely be exposed to both pre-dispersal and postdispersal insectpredators(Bagchietal2011)Wewerecarefultoclassifydepreda-tionstatusonthebasisofthepredatorthatweinitiallyrecordedtohaveattackedtheseedseedling(LewisampGripenberg2008)Thusaseedwithinsectentryexitholesattheinitialcensusthatwassub-sequentlypartiallyeatenorremovedbyvertebrateswasscoredas
predatedbyinsectsDuetothedifficultyinascertainingtheinitialpredatorbetweeninsectsandfungalpathogenswecollapsedthemintothenon-vertebratecategoryWethususedtwopredatorcat-egoriesvertebrateversusnon-vertebrate
WemeasuredasetofecologicalcovariatesthatcanpotentiallyinfluencevariousstagesofseedlingrecruitmentandthusshouldbeaccountedforinexaminingtheimpactsofloggingThesecovariatesincludedthreemeasuresoftreesizethataredeterminantsofseedcropsizeanddispersaldistanceDBHheightandcrowndiameter(CousensDythamampLaw2008NorghauerNockampGrogan2011)We also measured percentage canopy cover as a proxy for lightavailabilitywhich in turnmay influencegerminationand seedlingsurvival(Kobe1999)SeeSupportinginformationAppendixS1fordetailsonthesemeasurements
25emsp|emspStatistical analyses
Wefirstusedprincipal-componentsanalysis(PCA)toidentifymajortrends intreesizedataandreducethenumberofvariablesrepre-sentingtreesizeThefirstprincipalcomponent(PC1)waspositivelycorrelatedwithallthreevariablesrepresentingtreesizehadanei-genvaluegt1andexplained764ofthetotalvarianceintreesizedata (Supporting information Table S1) We used the componentscoresgeneratedfromthe loadingsofPC1asasurrogatefor treesizeinfurtherstatisticalanalyses
Wethenusedgeneralizedlinearmixedmodels(GLMMs)toana-lyzetheimpactsofloggingonseedcropsizeanddispersalpatternsusingthenumberofseeds ineachseedtrapastheresponsevari-ableWeusedforesttype(unloggedvslogged)distancefromthefocaltreePC1(hereafterldquotreesizerdquo)andalltwo-wayinteractionsbetween forest type and the other variables as fixed effectsWeincluded individualseedtrapsnestedwithintreesasa random in-terceptinallmodelsWeassumedaPoissonerrordistributionandaloglinkfunctionWetestedforoverdispersionbycalculatingthesumofsquaredPearsonresidualsandcomparing it totheresidualdegreesoffreedomforeachmodel(ZuurIenoWalkerSavelievampSmith2009)
WealsousedGLMMstoanalyzetheimpactofloggingontherelative role of vertebrates versus non-vertebrates inD lanceo-lataseedandseedlingpredationOurobservationsindicatedthatmostseedlingsdiedfrompredation(eguprootedandpartiallycompletelyconsumedremovedbyvertebratescotyledonsofger-minatedseedlingsdestroyedbyinsectsandorfungalpathogens)rather than from leaf damage typically inflicted by herbivores(ColeyampBarone1996)Thereforewepooleddataon seedandseedling predation For the natural plotswe scored each seedseedling as depredated by either vertebrate or non-vertebratepredators and then modeled the probability of a seedseedlingbeingdepredatedbyvertebrates (relative tonon-vertebrates)asa functionof forest typeas the fixedeffectvariableForpairedexperimental and controlplotswecounted thenumberofdep-redated seedsseedlings out of the total number of seeds andthenmodeledtheprobabilityofseedseedlingpredationWeused
8236emsp |emsp emspensp PILLAY et AL
foresttypeandtreatmenttype(experimentalvscontrolplots)asfixedeffectvariablesInbothanalysesofseedseedlingpredationweincludedindividualplotssequentiallynestedwithintransectsandtreesasarandominterceptWeassumedabinomialerrordis-tribution and a logit link functionWe note that nomadic herdsof bearded pigs destroyed our experimental exclosures for fourout of seven trees in unlogged forest (but not in logged forest)between1and19October(~30daysfromtheonsetofseedseed-lingmonitoringintheseplots)Thereforeforunloggedforestweonly considered data from the paired experimental and controlplotsforthethreetreesthatwerenotdepredatedbybeardedpigs(n=330seeds12plots)
WeusedCoxregressionmixed-effectssurvivalmodelstoan-alyzethe impactof loggingongerminationandseedlingsurvivalatthelevelofindividualseedsandseedlingswithdatacollectedfromthenaturalplotsWefirstmodeledseedsurvivaluntilger-minationwithsurvivalmodeledasdailygerminationrateOftheseeds that germinatedwe subsequentlymodeled daily seedlingsurvivaluntil3monthsafterseedfallWeincorporatedseedseed-lingageandusedright-censoring ifaseedseedlingsurvivedbe-yondtheendofthemonitoringperiodForfixedeffectvariablesweincludedforesttypelocal-scale(1m2)conspecificseedseed-lingdensity (hereafter ldquoconspecificseeddensityrdquo)distancefromthe parent tree and percentage canopy coverWe also includedtree size and total conspecific seedfall at each tree during thestudy (surrogate formedium-scale seed density) as fixed effectvariables because these factorsmay vary between the two for-esttypesandpotentiallyinfluenceseedlingrecruitmentpatterns(Bagchi etal 2011 CurranampWebb 2000) Lastlywe includedinteractions between forest type and the five latter variablesForrandomeffectswesequentiallynestedtheidentitiesofplotswithintransectsandtreestocontrolforpotentialvariationinmi-crotopographythatcouldcausedifferentialgerminationandseed-lingsurvival(Bornetal2015)
Fortheanalysesdescribedabovewebuiltsetsofsub-modelsbasedontheglobalmodelandcomparedmodelsusingAkaikersquos
Information Criterion adjusted for sample size (AICc) (BurnhamampAnderson2002)WeconsideredmodelsfromthelowestAICc until thecumulativemodelweightexceeded95Wethenusedthis95confidencemodelsetasthebasisformodelaveragingandstatisticalinference(BurnhamampAnderson2002)Weconductedall statistical analyses inR (v 321) (RDevelopmentCoreTeam2017)andusedtheglmer function in thepackageldquolme4rdquo (BatesMaumlchler Bolker ampWalker 2015) to fit all GLMMs the packageldquocoxmerdquo(Therneau2015)tofitsurvivalmodelsandthepackageldquoMuMInrdquo(Bartoń2016)formodelselectionandaveraging
3emsp |emspRESULTS
31emsp|emspImpact of logging on seed crop size
ThefivemostparsimoniousmodelswithacumulativeAICcweightof100(Supporting informationTableS2) indicatedthat foresttypedistancefromthefocaltreetreesizeandinteractionsbe-tweenforesttypeandtheothervariableshadsupportinexplain-ingvariationinD lanceolataseedcropsizeanddispersalpatternsConsistentwithprediction1theseedcroptendedtobesmallerin logged forest than in unlogged forest evenwhen accountingfor tree size (Figure3a Table1a)Over ~3months (85days)wecollected2105(n=168traps)and718(n=144traps)seedsinun-loggedandloggedforestrespectivelyTheaverageseeddensity(plusmn1SE) inunloggedforestwas1252(plusmn099)seedsm2comparedwith498(plusmn048)seedsm2inloggedforestThenumberofseedsdeclinedwithincreasingdistancefromthefocaltreesinbothfor-est types (Figure3bTable1a)Consistentwithpatternsof localseed dispersal (Itoh etal 1997) only 06of all trapped seedslanded at 32m in unlogged forest and none in logged forestLarger trees tended toproducemoreseeds inboth forest types(Figure3cTable1a)althoughtreesinloggedforestweresmallerthanthoseinunloggedforest(SupportinginformationFigureS1)Wefoundnoevidenceforoverdispersion(SupportinginformationTableS3)
F IGURE 3emspTherelationshipbetweenD lanceolataseeddensityand(a)foresttype(b)distancefromfocaltreesineachforesttypeand(c)treesizeineachforesttypeErrorbarsandtheshadedregionsofthecurvesarethepredicted95confidenceintervals
(a) (b) (c)
emspensp emsp | emsp8237PILLAY et AL
32emsp|emspImpact of logging on the predation of seeds and seedlings
Over3monthswerecordedanoverallseedandseedlingpredationrate of 866 and 836 in unlogged (n=1423 seeds 140 naturalplots)andlogged(n=646seeds120naturalplots)forestrespec-tivelyAsmallnumberofseeds(unloggedforest5loggedforest8)diedofdesiccationConsistentwithprediction2therewasashiftinthefunctionalroleofseedpredatorsawayfromnon-vertebratesto-wardvertebratesinloggedforest(Figure4ab)Inthenaturalplotsthe log odds of a seedseedling being depredated by vertebrates(relativetonon-vertebrates)werehigherinloggedforestthaninun-loggedforest(βlogged079SE05095CIminus028to185Figure4aSupportinginformationTableS4)Furthersupportingprediction2the logoddsofseedandseedlingpredationwere lower intheex-perimentalexclosureplotsthaninthecontrolplotsinloggedforest(βlogged-exclosureminus210SE05795CIminus343 tominus097Figure4b)In contrast the effect of exclosure treatments on seed predationtendedtobeweakerinunloggedforest(βunlogged-exclosureminus102SE 08895CIminus290to089Figure4bSupportinginformationTableS5)
33emsp|emspImpact of logging on density- dependent germination and seedling survival
We monitored the germination and survival status of seeds thatwerealiveinthenaturalplotsatthefirstcensus(603and227seedsin unlogged and logged forest respectively) until the end of thestudy The sixmost parsimoniousmodelswith a cumulativeAICcweightof97(SupportinginformationTableS6)indicatedthatfor-est type conspecific seed density distance from the parent treeseedfall tree size canopy cover and interactions between foresttypeandtheothervariableshadsupport inexplainingvariation inseedgerminationSeedsfacedgreaterhazard(iehigherprobabilityofmortality) inloggedforestthaninunloggedforest(Table1b)as471ofseedsfailedtogerminateinloggedforestcomparedwith08 in unlogged forestHigher conspecific seed densitywas as-sociatedwithlowerseedmortalityinunloggedforestandthisrela-tionshipalsotendedtoapplyinloggedforest(Figure5aTable1b)With increasingdistancefromparenttreesseedmortalitytendedto increase in both forest types but this relationshipwasweakerin logged forest (Figure5b Table1b) Higher seedfall and largertreesizetendedtobeassociatedwithlowerseedmortalityinbothforest types (Figure5cdTable1b)With increasing canopy coverseedmortality tended to increase inboth forest types (Figure5eTable1b)
Forexplainingvariationinseedlingsurvivalthetwomostparsi-moniousmodelswithacumulativeAICcweightof99(SupportinginformationTableS7) indicated that forest type conspecific seeddensity distance from the parent tree seedfall tree size canopycoverandinteractionsbetweenforesttypeandtheothervariableshad support Of the seeds that germinated seedlings tended tohavelowerprobabilityofmortalityinloggedforestthaninunlogged
forest(Table1c)as817ofgerminatedseedlingssurviveduptotheendofthestudyinloggedforestcomparedwith311inunloggedforestHigherconspecificseedlingdensitytendedtobeassociatedwithhigherseedlingmortality inunloggedforestbut inconsistentwith prediction 3 this relationship was reversed in logged forest(Figure5f Table1c) With increasing distance from parent treesseedlingmortalityincreasedinunloggedforestbutthisrelationshiptendedtobereversedinloggedforest(Figure5gTable1c)Higherseedfall tended tobe associatedwithhigher seedlingmortality inunloggedforestbutthisrelationshipalsotendedtobereversedinloggedforest(Figure5hTable1c)Likegerminationlargertreesizetendedtobeassociatedwithlowerseedlingmortalityinbothforesttypesandthisrelationshipwasstrongerinloggedforest(Figure5iTable1c)With increasingcanopycoverseedlingmortalitytendedtoincreaseinunloggedforestbutthisrelationshiptendedtobere-versedinloggedforest(Figure5jTable1c)
4emsp |emspDISCUSSION
Ourresultsdemonstratehowmultiplestagesoftheseedlingrecruit-mentprocessofacanopytreespeciesmaybealteredwhentropicalforestsaredegradedbyintensiveldquoselectiverdquologgingConsistentwithourpredictions the remaining reproductive trees in logged forestproducedamarkedlysmallerseedcropthanthetreesinunloggedforestevenafteraccountingfortreesizeandthefunctionalroleofvertebratesinseedpredationincreasedinloggedforestwhilethatof non-vertebrates declined The strength of density-dependencein dipterocarpsmay change frompositive to negative at differentlife stages (Blundell amp Peart 2004 Curran ampWebb 2000) Thisappearedtobethecase inunloggedforestwheregermination in-creasedwithlocal-scaleconspecificseeddensitypossiblybecausepredatorsweresatiatedbythehighmast-fruitingseeddensitiesbutseedlingsurvivaltendedtodecline(Figure5afTable1bc)HoweverinconsistentwithourpredictionofstrongerNDDinloggedforestgermination and especially seedling survival increasedwith local-scaleconspecificseeddensitywhichsuggeststhatloggingmayhaveaffectedpredator-mediatedNDDduringtheseed-to-seedlingtran-sitionbottleneck inD lanceolata Importantlyourfindingsappliedtoamast-fruitingyearwhenmostdipterocarprecruitmentoccurs(CurranampLeighton2000Janzen1974)suggestingthat intensiveloggingmaypotentiallyaffectlong-termpopulationdynamicsofD lanceolataOur findings add to knowledge of how ecological pro-cesses responsible for themaintenanceofbiodiversitymaybeaf-fectedbylogging(DarrigodosSantosampVenticinque2018Ewersetal2015Schleuningetal2011Woodcocketal2013)
Increasing edaphic and drought stress in reproducing treesin logged forest may have contributed to the reduced seed crop(Curran etal 1999 Hardwick etal 2015) The consequences ofseed limitation in logged forests for sapling and ultimately adulttree recruitment remain largelyunexploredbutmaybedetrimen-tal for long-term tree population dynamics (Caughlin etal 2015)Changes in the functional roles of non-vertebrate seed predators
8238emsp |emsp emspensp PILLAY et AL
relativetovertebratesinloggedforestmaybedrivenbynumericalchanges inpredatorabundanceacrossgroups (Ewersetal2015)The altered microclimatic conditions in logged forests are likelyhostile to populations of insect seed predators and fungal patho-gens(Ewersetal2015Hardwicketal2015)Converselylogged
forestsmayprovideincreasedresourceavailabilityforrodentseedpredatorsandthusbenefittheirpopulations(Ewersetal2015)
Theuniqueecologyofmast-fruitingandtheimpactthisphenom-enonmayhavesustainedinloggedforestmayexplainthecomplexdensity-dependent patterns of germination and seedling survival(Figure5af)On theonehand in unlogged forest predator satia-tionmayhavebeenoccurringatthehighseeddensitiesduringthemast(Janzen1970)aspotentiallysupportedbyourfindingthatger-minationtendedtoincreasewithhigherseedfall(Figure5cBagchietal2011CurranampWebb2000)Indeedmast-fruitinghasbeenhypothesizedtobeanevolutionaryresponsetodensity-dependentmortality factors allowing seeds to escape predation by satiatingseedpredators (Janzen19701974)Ontheotherhand in loggedforesttheconcentratedseeddensitiesunderspatiallyisolatedadulttreesmayallowNDDtooperate(Bagchietal2011CurranampWebb2000)Howeverourfindingsofincreasedgerminationandespeciallyseedlingsurvivalwithhigherconspecificseeddensityinloggedfor-est(Figure5afTable1bc)werecontrarytotheexpectationsunderNDDandmaybeassociatedwiththediminishedfunctionalroleofnon-vertebrate seedpredators in logged forest (Figure4)NDD isprimarily driven by host-specific insect seed predators and fungalpathogenswhichtendtoconcentrateamongthehigh-seedseedingdensitiesunderthecrownsofparenttreestherebycausinghighermortalitywhere densities are higher (Bagchi etal 2014 Connell1971 Janzen 1970) These non-vertebrate seed predators andpathogensmaybedeclining in logged forests (Ewers etal 2015)andtheirecologicalroleinmaintainingNDDmaybediminishedIncontrastthetendencyofvertebratestoforageoverlargeareasmayrender predation-relatedmortality to bemore spatially heteroge-neousrelativetoseedseedlingdensities(SwamyampTerborgh2010)
Wenotethatseedcropsizegerminationandseedlingsurvivaltendedtoincreaseforlargertreesinbothforesttypes(Figures3c5di)Thissuggeststhatselectiveloggingpracticesthatharvesttim-ber at sustainable rates and followsilviculturalpracticesdesignedtominimizedamagetotheresidualstand(Asneretal2009Martinetal2015Putzetal2012)arecriticaltopreventseedlingrecruit-mentfailure indipterocarpforestsSeedgerminationandseedlingsurvivalofD lanceolatatendstobepositivelyassociatedwithlightavailability (Itoh etal 1995) which likely explains why seed andseedling mortality tended to increase with higher canopy cover(Figure5ej)
41emsp|emspCaveats and limitations
OurstudyincludedsevenandsixD lanceolatatreesasindepend-ent experimental units in unlogged and logged forests respec-tively (cfBagchietal2011HolbrookampLoiselle2009Poulsenetal 2012) The spatially clumped distributions of most adultfruiting individuals inunlogged forestand the fewspatially scat-teredadultdipterocarpsremaininginloggedforest(ofallspeciesD lanceolata was the most abundant at seven individuals) pre-cludedadditionalreplicationatthelevelofindividualtreeswithinforesttypeThesparsenumberofadultdipterocarpsinthelogged
TABLE 1emspModelaveragedestimatesexplainingvariationin(a)seedcropsize(b)germinationand(c)seedlingsurvival(upto3monthsafterseedfall)ofD lanceolatainrelationtothepredictorvariablesthatweresupportedbyAICc-basedmodelselectioncriteria(SupportinginformationTablesS2S6S7)
Response and predictor variables Estimate (SE) 95 CI
(a)Seedcropsize
Intercept 300(029) 240ndash352
Loggedforest minus080(048) minus172ndash007
Distance minus013 (001) minus014tominus011
Loggedforesttimesdistance minus001(001) minus005ndash001
Treesize 006(014) minus018ndash060
Loggedforesttimestreesize 001(010) minus054ndash080
(b)Germination
Logged forest 468 (362) 269ndash1096
Conspecific seed density minus271 (238) minus744tominus075
Logged foresttimesconspecific seed density
265 (235) 105ndash723
Distance 003(018) minus062ndash133
Loggedforesttimesdistance minus002(016) minus134ndash091
Seedfall minus084(157) minus602ndash104
Loggedforesttimesseedfall 024(149) minus422ndash1428
Treesize minus018(098) minus639ndash329
Loggedforesttimestreesize minus014(108) minus1072ndash474
Canopycover 001(032) minus217ndash255
Loggedforesttimescanopycover 015(084) minus155ndash775
(c)Seedlingsurvival
Loggedforest minus710(403) minus1500ndash081
Conspecificseedlingdensity 030(015) minus001ndash060
Logged foresttimesconspecific seedling density
minus170 (043) minus255tominus086
Distance 015 (009) 002ndash032
Logged foresttimesdistance minus104 (067) minus231 tominus012
Seedfall 003(058) minus119ndash126
Loggedforesttimesseedfall minus203(307) minus863ndash389
Treesize minus003(096) minus206ndash199
Logged foresttimestree size minus316 (205) minus706 tominus033
Canopycover 027(028) minus024ndash087
Loggedforesttimescanopycover minus034(110) minus271to191
NotesResultsforseedcropsizerepresentcoefficients(log-scale)esti-matedwithgeneralizedlinearmixedmodelsResultsforgerminationandseedling survival represent loghazardsestimatedwithCox regressionmixed-effectssurvivalmodelsEstimatesinitalicsindicatethatthe95confidenceintervalsdidnotoverlapzerosuggestingastrongeffectofthepredictorvariableonthecorrespondingresponsevariable
emspensp emsp | emsp8239PILLAY et AL
forestisareflectionofthepopulationreductionmanytimbertreespeciesaresubjected toafter intensiveselective logging (Martinetal2015)
The variable density of adultD lanceolata trees between un-logged and logged forests may introduce confounding negativedensity-dependentneighbourhoodeffectsonseedlingrecruitment(BlundellampPeart2004StollampNewbery2005)PreviousresearchontheDipterocarpaceaesuggeststhatneighbourhoodeffectsmayoccurwhenconspecificadultsarewithin20mofeachother(StollampNewbery2005)Ourrequirementofnon-overlappingseedshad-owsbetweenfocaltreesensuredthattreeswereseparatedbyatleast40mTherelativelylargerdistancebetweenthefocaltreesinourstudycomparedwiththethresholddistanceof20matwhichneighbourhoodeffectsmayoccur(StollampNewbery2005)shouldthusservetominimizethispotentialconfoundingfactor
Inanalyzingagentsofseedandseedlingpredationwedidnotdistinguishbetweenthedifferentprocessesofseedlingpredation
andherbivoryOftheseedlingsthatwerealiveinthenaturalplotsat the end of the study 017 and 176 showed signs of leafdamagetypicalofinsectherbivory(ColeyampBarone1996)inun-loggedandloggedforestsrespectively Intheexperimentalandpairedcontrolplotsthepercentageofseedlingswithsignsofleafdamage fromherbivorywas similarly small (061and065 inunloggedand logged forest respectively)Thusobservedseed-lingherbivoryrateswerelowAlonger-termstudymayrevealal-teredseedlingherbivoryrateswithlogging(Darrigoetal2018)particularly because herbivorous insect biomass was found toincrease with logging (Ewers etal 2015) Our study examinestheeffectsofintensiveselectiveloggingontheseed-to-seedlingtransitionphaseofacanopydipterocarpHoweverour findingsmaynot represent the fateofseedlingsovera longer timespanbecause ecological changes caused by logging (eg herbivory)could continue to impact the survival of seedlings beyond theseed-to-seedlingtransitionbottleneck(Caughlinetal2015)
F IGURE 4emspTheoddsofpredationofD lanceolataseedsbyvertebratesrelativetonon-vertebratesin(a)naturalplotsand(b)experimental(vertebrateexclosures)andpairedcontrolplotsinunloggedandloggedforestErrorbarsrepresent95confidenceintervals
(a) (b)
F IGURE 5emspTherelationshipsbetweenD lanceolataseedgermination(toppanel)seedlingsurvival(bottompanel)and(af)conspecificseedseedlingdensity(bg)distancefromtheparenttree(ch)seedfall(di)treesizeand(ej)canopycoverinunloggedandloggedforests
(a) (b) (c) (d) (e)
(f) (g) (h) (i) (j)
8240emsp |emsp emspensp PILLAY et AL
WedidnotmanipulatedensityanddistanceindependentlyOuruseof seeddensity gradientsnaturally generatedby thedistancegradient can identify density-dependent patterns of seedling re-cruitment (Harms etal 2000Webbamp Peart 1999)However intheabsenceofexperimentalmanipulationofdensityanddistanceeffects independent of each other our ability to understand thecauses underlying observed patterns of density-dependence inunloggedand logged forests is limited (SwamyampTerborgh2010)Futurestudiesshouldleveragemanipulativeexperimentsforanu-ancedunderstandingof the causes underlying alteredpatterns ofseedling recruitment in the face of anthropogenic disturbances(FreckletonampLewis2006)
5emsp |emspCONCLUSION
We found that for Dryobalanops lanceolata a dipterocarp spe-ciesendangeredby thecommercial timber trade (Ashton1998)multiple stages of seedling recruitment were altered in selec-tively logged forest compared with unlogged forest during amast-fruiting year Future studies should leverage broader log-ging gradients additional species and experimental approachesover longer time frames (Bagchietal2011Martinetal2015Riuttaetal2018Struebigetal2013SwamyampTerborgh2010)to quantify the thresholds of logging intensity abovewhich theecologicalprocessofseedlingrecruitmentmayunravelWehigh-lighttheimportanceofunderstandingtheimpactsofdisturbancessuch as logging on ecological processeswhich can complementnumericalassessmentsofbiodiversitytounmaskimpactsthatmayotherwiseremainhidden
ACKNOWLEDG MENTS
We thank Yayasan Sabah BentaWawasan Sdn Bhd the SabahBiodiversity Council the Sabah Forestry Department theMaliauBasin Management Committee the State Secretary Sabah ChiefMinisterrsquosDepartmenttheMalaysianEconomicPlanningUnitandtheRoyalSocietySouthEastAsiaRainforestResearchPartnershipfor granting permits Our fieldwork was funded by grants fromthe Rufford Small Grants Foundation IDEAWild the Institute ofFoodandAgriculturalSciencesandtheTropicalConservationandDevelopmentProgramattheUniversityofFloridaWethankRyanGray andMinSheng Khoo for coordinating field logistics MainusTausong JeffryAminMohdYusufDidin (Roy)RismanAjangandMelvin Teronggoh for assistance during fieldwork Magat JaparandJeffryAminfor identifyingtreesseedsandseedlingsJeffreyHostetler forhelpwith survival analysis andEmilioBrunaTrevorCaughlin David Newbery and one anonymous reviewer for con-structivecommentsthatgreatlyimprovedthemanuscript
CONFLIC T OF INTERE S T
Nonedeclared
AUTHOR CONTRIBUTIONS
RPconceivedthisstudyRPandRJFraisedthegrantsforfieldworkRPBALRJFandHBdesignedthemethodologyRPcollectedthedataandperformedallstatisticalanalysesRPandFHledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandprovidedfinalapprovalforpublication
DATA ACCE SSIBILIT Y
DatacanbeaccessedthroughtheDryadDigitalRepositoryhttpsdoiorg105061dryaddk4t694 (Pillay Hua Loiselle Bernard ampFletcher2018)
ORCID
Rajeev Pillay httporcidorg0000-0002-7116-6855
R E FE R E N C E S
AshtonP (1998)Dryobalanops lanceolatahttpwwwiucnredlistorgdetails331640(accessed11March2015)
Asner G P Rudel T K Aide T M Defries R amp Emerson R(2009) A contemporary assessment of change in humid trop-ical forests Conservation Biology 23 1386ndash1395 httpsdoiorg101111j1523-1739200901333x
BagchiRGalleryREGripenbergSGurrSJNarayanLAddisCEhellipLewisOT(2014)Pathogensandinsectherbivoresdriverain-forestplantdiversityandcompositionNature50685ndash88httpsdoiorg101038nature12911
Bagchi R Philipson C D Slade E M Hector A Phillips SVillanueva J F hellip Press M C (2011) Impacts of logging ondensity-dependentpredationofdipterocarpseedsinaSouthEastAsian rainforestPhilosophical Transactions of the Royal Society B Biological Sciences 366 3246ndash3255 httpsdoiorg101098rstb20110034
Bartoń K (2016) MuMIn Multi-model inference R package version 1156
BatesDMaumlchlerMBolkerBMampWalkerSC(2015)Fittinglinearmixed-effectsmodelsusing lme4Journal of Statistical Software67httpsdoiorg1018637jssv067i01
BlundellAGampPeartDR(2004)Density-dependentpopulationdy-namicsofadominantrainforestcanopytreeEcology85704ndash715httpsdoiorg10189001-4101
BornJBagchiRBurslemDNilusRTellenbachCPluessARampGhazoulJ(2015)DifferentialresponsesofdipterocarpseedlingstosoilmoistureandmicrotopographyBiotropica4749ndash58httpsdoiorg101111btp12180
BrunaEM (1999) Seedgermination in rainforest fragmentsNature402139httpsdoiorg10103845963
BurnhamKPampAndersonDR(2002)Model Selection and Multimodel Inference A Practical Information-Theoretic ApproachNewYorkNYSpringer-Verlaghttpsdoiorg101007b97636
Caughlin T T Ferguson J M Lichstein J W Zuidema P ABunyavejchewinSampLeveyD J (2015)Lossofanimal seeddis-persalincreasesextinctionriskinatropicaltreespeciesduetoper-vasivenegativedensitydependenceacross life stagesProceedings of the Royal Society B Biological Sciences28220142095httpsdoiorg101098rspb20142095
ChambersJCampMacMahonJA (1994)Adayinthe lifeofaseedMovementsandfatesofseedsandtheirimplicationsfornaturaland
emspensp emsp | emsp8241PILLAY et AL
managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
8236emsp |emsp emspensp PILLAY et AL
foresttypeandtreatmenttype(experimentalvscontrolplots)asfixedeffectvariablesInbothanalysesofseedseedlingpredationweincludedindividualplotssequentiallynestedwithintransectsandtreesasarandominterceptWeassumedabinomialerrordis-tribution and a logit link functionWe note that nomadic herdsof bearded pigs destroyed our experimental exclosures for fourout of seven trees in unlogged forest (but not in logged forest)between1and19October(~30daysfromtheonsetofseedseed-lingmonitoringintheseplots)Thereforeforunloggedforestweonly considered data from the paired experimental and controlplotsforthethreetreesthatwerenotdepredatedbybeardedpigs(n=330seeds12plots)
WeusedCoxregressionmixed-effectssurvivalmodelstoan-alyzethe impactof loggingongerminationandseedlingsurvivalatthelevelofindividualseedsandseedlingswithdatacollectedfromthenaturalplotsWefirstmodeledseedsurvivaluntilger-minationwithsurvivalmodeledasdailygerminationrateOftheseeds that germinatedwe subsequentlymodeled daily seedlingsurvivaluntil3monthsafterseedfallWeincorporatedseedseed-lingageandusedright-censoring ifaseedseedlingsurvivedbe-yondtheendofthemonitoringperiodForfixedeffectvariablesweincludedforesttypelocal-scale(1m2)conspecificseedseed-lingdensity (hereafter ldquoconspecificseeddensityrdquo)distancefromthe parent tree and percentage canopy coverWe also includedtree size and total conspecific seedfall at each tree during thestudy (surrogate formedium-scale seed density) as fixed effectvariables because these factorsmay vary between the two for-esttypesandpotentiallyinfluenceseedlingrecruitmentpatterns(Bagchi etal 2011 CurranampWebb 2000) Lastlywe includedinteractions between forest type and the five latter variablesForrandomeffectswesequentiallynestedtheidentitiesofplotswithintransectsandtreestocontrolforpotentialvariationinmi-crotopographythatcouldcausedifferentialgerminationandseed-lingsurvival(Bornetal2015)
Fortheanalysesdescribedabovewebuiltsetsofsub-modelsbasedontheglobalmodelandcomparedmodelsusingAkaikersquos
Information Criterion adjusted for sample size (AICc) (BurnhamampAnderson2002)WeconsideredmodelsfromthelowestAICc until thecumulativemodelweightexceeded95Wethenusedthis95confidencemodelsetasthebasisformodelaveragingandstatisticalinference(BurnhamampAnderson2002)Weconductedall statistical analyses inR (v 321) (RDevelopmentCoreTeam2017)andusedtheglmer function in thepackageldquolme4rdquo (BatesMaumlchler Bolker ampWalker 2015) to fit all GLMMs the packageldquocoxmerdquo(Therneau2015)tofitsurvivalmodelsandthepackageldquoMuMInrdquo(Bartoń2016)formodelselectionandaveraging
3emsp |emspRESULTS
31emsp|emspImpact of logging on seed crop size
ThefivemostparsimoniousmodelswithacumulativeAICcweightof100(Supporting informationTableS2) indicatedthat foresttypedistancefromthefocaltreetreesizeandinteractionsbe-tweenforesttypeandtheothervariableshadsupportinexplain-ingvariationinD lanceolataseedcropsizeanddispersalpatternsConsistentwithprediction1theseedcroptendedtobesmallerin logged forest than in unlogged forest evenwhen accountingfor tree size (Figure3a Table1a)Over ~3months (85days)wecollected2105(n=168traps)and718(n=144traps)seedsinun-loggedandloggedforestrespectivelyTheaverageseeddensity(plusmn1SE) inunloggedforestwas1252(plusmn099)seedsm2comparedwith498(plusmn048)seedsm2inloggedforestThenumberofseedsdeclinedwithincreasingdistancefromthefocaltreesinbothfor-est types (Figure3bTable1a)Consistentwithpatternsof localseed dispersal (Itoh etal 1997) only 06of all trapped seedslanded at 32m in unlogged forest and none in logged forestLarger trees tended toproducemoreseeds inboth forest types(Figure3cTable1a)althoughtreesinloggedforestweresmallerthanthoseinunloggedforest(SupportinginformationFigureS1)Wefoundnoevidenceforoverdispersion(SupportinginformationTableS3)
F IGURE 3emspTherelationshipbetweenD lanceolataseeddensityand(a)foresttype(b)distancefromfocaltreesineachforesttypeand(c)treesizeineachforesttypeErrorbarsandtheshadedregionsofthecurvesarethepredicted95confidenceintervals
(a) (b) (c)
emspensp emsp | emsp8237PILLAY et AL
32emsp|emspImpact of logging on the predation of seeds and seedlings
Over3monthswerecordedanoverallseedandseedlingpredationrate of 866 and 836 in unlogged (n=1423 seeds 140 naturalplots)andlogged(n=646seeds120naturalplots)forestrespec-tivelyAsmallnumberofseeds(unloggedforest5loggedforest8)diedofdesiccationConsistentwithprediction2therewasashiftinthefunctionalroleofseedpredatorsawayfromnon-vertebratesto-wardvertebratesinloggedforest(Figure4ab)Inthenaturalplotsthe log odds of a seedseedling being depredated by vertebrates(relativetonon-vertebrates)werehigherinloggedforestthaninun-loggedforest(βlogged079SE05095CIminus028to185Figure4aSupportinginformationTableS4)Furthersupportingprediction2the logoddsofseedandseedlingpredationwere lower intheex-perimentalexclosureplotsthaninthecontrolplotsinloggedforest(βlogged-exclosureminus210SE05795CIminus343 tominus097Figure4b)In contrast the effect of exclosure treatments on seed predationtendedtobeweakerinunloggedforest(βunlogged-exclosureminus102SE 08895CIminus290to089Figure4bSupportinginformationTableS5)
33emsp|emspImpact of logging on density- dependent germination and seedling survival
We monitored the germination and survival status of seeds thatwerealiveinthenaturalplotsatthefirstcensus(603and227seedsin unlogged and logged forest respectively) until the end of thestudy The sixmost parsimoniousmodelswith a cumulativeAICcweightof97(SupportinginformationTableS6)indicatedthatfor-est type conspecific seed density distance from the parent treeseedfall tree size canopy cover and interactions between foresttypeandtheothervariableshadsupport inexplainingvariation inseedgerminationSeedsfacedgreaterhazard(iehigherprobabilityofmortality) inloggedforestthaninunloggedforest(Table1b)as471ofseedsfailedtogerminateinloggedforestcomparedwith08 in unlogged forestHigher conspecific seed densitywas as-sociatedwithlowerseedmortalityinunloggedforestandthisrela-tionshipalsotendedtoapplyinloggedforest(Figure5aTable1b)With increasingdistancefromparenttreesseedmortalitytendedto increase in both forest types but this relationshipwasweakerin logged forest (Figure5b Table1b) Higher seedfall and largertreesizetendedtobeassociatedwithlowerseedmortalityinbothforest types (Figure5cdTable1b)With increasing canopy coverseedmortality tended to increase inboth forest types (Figure5eTable1b)
Forexplainingvariationinseedlingsurvivalthetwomostparsi-moniousmodelswithacumulativeAICcweightof99(SupportinginformationTableS7) indicated that forest type conspecific seeddensity distance from the parent tree seedfall tree size canopycoverandinteractionsbetweenforesttypeandtheothervariableshad support Of the seeds that germinated seedlings tended tohavelowerprobabilityofmortalityinloggedforestthaninunlogged
forest(Table1c)as817ofgerminatedseedlingssurviveduptotheendofthestudyinloggedforestcomparedwith311inunloggedforestHigherconspecificseedlingdensitytendedtobeassociatedwithhigherseedlingmortality inunloggedforestbut inconsistentwith prediction 3 this relationship was reversed in logged forest(Figure5f Table1c) With increasing distance from parent treesseedlingmortalityincreasedinunloggedforestbutthisrelationshiptendedtobereversedinloggedforest(Figure5gTable1c)Higherseedfall tended tobe associatedwithhigher seedlingmortality inunloggedforestbutthisrelationshipalsotendedtobereversedinloggedforest(Figure5hTable1c)Likegerminationlargertreesizetendedtobeassociatedwithlowerseedlingmortalityinbothforesttypesandthisrelationshipwasstrongerinloggedforest(Figure5iTable1c)With increasingcanopycoverseedlingmortalitytendedtoincreaseinunloggedforestbutthisrelationshiptendedtobere-versedinloggedforest(Figure5jTable1c)
4emsp |emspDISCUSSION
Ourresultsdemonstratehowmultiplestagesoftheseedlingrecruit-mentprocessofacanopytreespeciesmaybealteredwhentropicalforestsaredegradedbyintensiveldquoselectiverdquologgingConsistentwithourpredictions the remaining reproductive trees in logged forestproducedamarkedlysmallerseedcropthanthetreesinunloggedforestevenafteraccountingfortreesizeandthefunctionalroleofvertebratesinseedpredationincreasedinloggedforestwhilethatof non-vertebrates declined The strength of density-dependencein dipterocarpsmay change frompositive to negative at differentlife stages (Blundell amp Peart 2004 Curran ampWebb 2000) Thisappearedtobethecase inunloggedforestwheregermination in-creasedwithlocal-scaleconspecificseeddensitypossiblybecausepredatorsweresatiatedbythehighmast-fruitingseeddensitiesbutseedlingsurvivaltendedtodecline(Figure5afTable1bc)HoweverinconsistentwithourpredictionofstrongerNDDinloggedforestgermination and especially seedling survival increasedwith local-scaleconspecificseeddensitywhichsuggeststhatloggingmayhaveaffectedpredator-mediatedNDDduringtheseed-to-seedlingtran-sitionbottleneck inD lanceolata Importantlyourfindingsappliedtoamast-fruitingyearwhenmostdipterocarprecruitmentoccurs(CurranampLeighton2000Janzen1974)suggestingthat intensiveloggingmaypotentiallyaffectlong-termpopulationdynamicsofD lanceolataOur findings add to knowledge of how ecological pro-cesses responsible for themaintenanceofbiodiversitymaybeaf-fectedbylogging(DarrigodosSantosampVenticinque2018Ewersetal2015Schleuningetal2011Woodcocketal2013)
Increasing edaphic and drought stress in reproducing treesin logged forest may have contributed to the reduced seed crop(Curran etal 1999 Hardwick etal 2015) The consequences ofseed limitation in logged forests for sapling and ultimately adulttree recruitment remain largelyunexploredbutmaybedetrimen-tal for long-term tree population dynamics (Caughlin etal 2015)Changes in the functional roles of non-vertebrate seed predators
8238emsp |emsp emspensp PILLAY et AL
relativetovertebratesinloggedforestmaybedrivenbynumericalchanges inpredatorabundanceacrossgroups (Ewersetal2015)The altered microclimatic conditions in logged forests are likelyhostile to populations of insect seed predators and fungal patho-gens(Ewersetal2015Hardwicketal2015)Converselylogged
forestsmayprovideincreasedresourceavailabilityforrodentseedpredatorsandthusbenefittheirpopulations(Ewersetal2015)
Theuniqueecologyofmast-fruitingandtheimpactthisphenom-enonmayhavesustainedinloggedforestmayexplainthecomplexdensity-dependent patterns of germination and seedling survival(Figure5af)On theonehand in unlogged forest predator satia-tionmayhavebeenoccurringatthehighseeddensitiesduringthemast(Janzen1970)aspotentiallysupportedbyourfindingthatger-minationtendedtoincreasewithhigherseedfall(Figure5cBagchietal2011CurranampWebb2000)Indeedmast-fruitinghasbeenhypothesizedtobeanevolutionaryresponsetodensity-dependentmortality factors allowing seeds to escape predation by satiatingseedpredators (Janzen19701974)Ontheotherhand in loggedforesttheconcentratedseeddensitiesunderspatiallyisolatedadulttreesmayallowNDDtooperate(Bagchietal2011CurranampWebb2000)Howeverourfindingsofincreasedgerminationandespeciallyseedlingsurvivalwithhigherconspecificseeddensityinloggedfor-est(Figure5afTable1bc)werecontrarytotheexpectationsunderNDDandmaybeassociatedwiththediminishedfunctionalroleofnon-vertebrate seedpredators in logged forest (Figure4)NDD isprimarily driven by host-specific insect seed predators and fungalpathogenswhichtendtoconcentrateamongthehigh-seedseedingdensitiesunderthecrownsofparenttreestherebycausinghighermortalitywhere densities are higher (Bagchi etal 2014 Connell1971 Janzen 1970) These non-vertebrate seed predators andpathogensmaybedeclining in logged forests (Ewers etal 2015)andtheirecologicalroleinmaintainingNDDmaybediminishedIncontrastthetendencyofvertebratestoforageoverlargeareasmayrender predation-relatedmortality to bemore spatially heteroge-neousrelativetoseedseedlingdensities(SwamyampTerborgh2010)
Wenotethatseedcropsizegerminationandseedlingsurvivaltendedtoincreaseforlargertreesinbothforesttypes(Figures3c5di)Thissuggeststhatselectiveloggingpracticesthatharvesttim-ber at sustainable rates and followsilviculturalpracticesdesignedtominimizedamagetotheresidualstand(Asneretal2009Martinetal2015Putzetal2012)arecriticaltopreventseedlingrecruit-mentfailure indipterocarpforestsSeedgerminationandseedlingsurvivalofD lanceolatatendstobepositivelyassociatedwithlightavailability (Itoh etal 1995) which likely explains why seed andseedling mortality tended to increase with higher canopy cover(Figure5ej)
41emsp|emspCaveats and limitations
OurstudyincludedsevenandsixD lanceolatatreesasindepend-ent experimental units in unlogged and logged forests respec-tively (cfBagchietal2011HolbrookampLoiselle2009Poulsenetal 2012) The spatially clumped distributions of most adultfruiting individuals inunlogged forestand the fewspatially scat-teredadultdipterocarpsremaininginloggedforest(ofallspeciesD lanceolata was the most abundant at seven individuals) pre-cludedadditionalreplicationatthelevelofindividualtreeswithinforesttypeThesparsenumberofadultdipterocarpsinthelogged
TABLE 1emspModelaveragedestimatesexplainingvariationin(a)seedcropsize(b)germinationand(c)seedlingsurvival(upto3monthsafterseedfall)ofD lanceolatainrelationtothepredictorvariablesthatweresupportedbyAICc-basedmodelselectioncriteria(SupportinginformationTablesS2S6S7)
Response and predictor variables Estimate (SE) 95 CI
(a)Seedcropsize
Intercept 300(029) 240ndash352
Loggedforest minus080(048) minus172ndash007
Distance minus013 (001) minus014tominus011
Loggedforesttimesdistance minus001(001) minus005ndash001
Treesize 006(014) minus018ndash060
Loggedforesttimestreesize 001(010) minus054ndash080
(b)Germination
Logged forest 468 (362) 269ndash1096
Conspecific seed density minus271 (238) minus744tominus075
Logged foresttimesconspecific seed density
265 (235) 105ndash723
Distance 003(018) minus062ndash133
Loggedforesttimesdistance minus002(016) minus134ndash091
Seedfall minus084(157) minus602ndash104
Loggedforesttimesseedfall 024(149) minus422ndash1428
Treesize minus018(098) minus639ndash329
Loggedforesttimestreesize minus014(108) minus1072ndash474
Canopycover 001(032) minus217ndash255
Loggedforesttimescanopycover 015(084) minus155ndash775
(c)Seedlingsurvival
Loggedforest minus710(403) minus1500ndash081
Conspecificseedlingdensity 030(015) minus001ndash060
Logged foresttimesconspecific seedling density
minus170 (043) minus255tominus086
Distance 015 (009) 002ndash032
Logged foresttimesdistance minus104 (067) minus231 tominus012
Seedfall 003(058) minus119ndash126
Loggedforesttimesseedfall minus203(307) minus863ndash389
Treesize minus003(096) minus206ndash199
Logged foresttimestree size minus316 (205) minus706 tominus033
Canopycover 027(028) minus024ndash087
Loggedforesttimescanopycover minus034(110) minus271to191
NotesResultsforseedcropsizerepresentcoefficients(log-scale)esti-matedwithgeneralizedlinearmixedmodelsResultsforgerminationandseedling survival represent loghazardsestimatedwithCox regressionmixed-effectssurvivalmodelsEstimatesinitalicsindicatethatthe95confidenceintervalsdidnotoverlapzerosuggestingastrongeffectofthepredictorvariableonthecorrespondingresponsevariable
emspensp emsp | emsp8239PILLAY et AL
forestisareflectionofthepopulationreductionmanytimbertreespeciesaresubjected toafter intensiveselective logging (Martinetal2015)
The variable density of adultD lanceolata trees between un-logged and logged forests may introduce confounding negativedensity-dependentneighbourhoodeffectsonseedlingrecruitment(BlundellampPeart2004StollampNewbery2005)PreviousresearchontheDipterocarpaceaesuggeststhatneighbourhoodeffectsmayoccurwhenconspecificadultsarewithin20mofeachother(StollampNewbery2005)Ourrequirementofnon-overlappingseedshad-owsbetweenfocaltreesensuredthattreeswereseparatedbyatleast40mTherelativelylargerdistancebetweenthefocaltreesinourstudycomparedwiththethresholddistanceof20matwhichneighbourhoodeffectsmayoccur(StollampNewbery2005)shouldthusservetominimizethispotentialconfoundingfactor
Inanalyzingagentsofseedandseedlingpredationwedidnotdistinguishbetweenthedifferentprocessesofseedlingpredation
andherbivoryOftheseedlingsthatwerealiveinthenaturalplotsat the end of the study 017 and 176 showed signs of leafdamagetypicalofinsectherbivory(ColeyampBarone1996)inun-loggedandloggedforestsrespectively Intheexperimentalandpairedcontrolplotsthepercentageofseedlingswithsignsofleafdamage fromherbivorywas similarly small (061and065 inunloggedand logged forest respectively)Thusobservedseed-lingherbivoryrateswerelowAlonger-termstudymayrevealal-teredseedlingherbivoryrateswithlogging(Darrigoetal2018)particularly because herbivorous insect biomass was found toincrease with logging (Ewers etal 2015) Our study examinestheeffectsofintensiveselectiveloggingontheseed-to-seedlingtransitionphaseofacanopydipterocarpHoweverour findingsmaynot represent the fateofseedlingsovera longer timespanbecause ecological changes caused by logging (eg herbivory)could continue to impact the survival of seedlings beyond theseed-to-seedlingtransitionbottleneck(Caughlinetal2015)
F IGURE 4emspTheoddsofpredationofD lanceolataseedsbyvertebratesrelativetonon-vertebratesin(a)naturalplotsand(b)experimental(vertebrateexclosures)andpairedcontrolplotsinunloggedandloggedforestErrorbarsrepresent95confidenceintervals
(a) (b)
F IGURE 5emspTherelationshipsbetweenD lanceolataseedgermination(toppanel)seedlingsurvival(bottompanel)and(af)conspecificseedseedlingdensity(bg)distancefromtheparenttree(ch)seedfall(di)treesizeand(ej)canopycoverinunloggedandloggedforests
(a) (b) (c) (d) (e)
(f) (g) (h) (i) (j)
8240emsp |emsp emspensp PILLAY et AL
WedidnotmanipulatedensityanddistanceindependentlyOuruseof seeddensity gradientsnaturally generatedby thedistancegradient can identify density-dependent patterns of seedling re-cruitment (Harms etal 2000Webbamp Peart 1999)However intheabsenceofexperimentalmanipulationofdensityanddistanceeffects independent of each other our ability to understand thecauses underlying observed patterns of density-dependence inunloggedand logged forests is limited (SwamyampTerborgh2010)Futurestudiesshouldleveragemanipulativeexperimentsforanu-ancedunderstandingof the causes underlying alteredpatterns ofseedling recruitment in the face of anthropogenic disturbances(FreckletonampLewis2006)
5emsp |emspCONCLUSION
We found that for Dryobalanops lanceolata a dipterocarp spe-ciesendangeredby thecommercial timber trade (Ashton1998)multiple stages of seedling recruitment were altered in selec-tively logged forest compared with unlogged forest during amast-fruiting year Future studies should leverage broader log-ging gradients additional species and experimental approachesover longer time frames (Bagchietal2011Martinetal2015Riuttaetal2018Struebigetal2013SwamyampTerborgh2010)to quantify the thresholds of logging intensity abovewhich theecologicalprocessofseedlingrecruitmentmayunravelWehigh-lighttheimportanceofunderstandingtheimpactsofdisturbancessuch as logging on ecological processeswhich can complementnumericalassessmentsofbiodiversitytounmaskimpactsthatmayotherwiseremainhidden
ACKNOWLEDG MENTS
We thank Yayasan Sabah BentaWawasan Sdn Bhd the SabahBiodiversity Council the Sabah Forestry Department theMaliauBasin Management Committee the State Secretary Sabah ChiefMinisterrsquosDepartmenttheMalaysianEconomicPlanningUnitandtheRoyalSocietySouthEastAsiaRainforestResearchPartnershipfor granting permits Our fieldwork was funded by grants fromthe Rufford Small Grants Foundation IDEAWild the Institute ofFoodandAgriculturalSciencesandtheTropicalConservationandDevelopmentProgramattheUniversityofFloridaWethankRyanGray andMinSheng Khoo for coordinating field logistics MainusTausong JeffryAminMohdYusufDidin (Roy)RismanAjangandMelvin Teronggoh for assistance during fieldwork Magat JaparandJeffryAminfor identifyingtreesseedsandseedlingsJeffreyHostetler forhelpwith survival analysis andEmilioBrunaTrevorCaughlin David Newbery and one anonymous reviewer for con-structivecommentsthatgreatlyimprovedthemanuscript
CONFLIC T OF INTERE S T
Nonedeclared
AUTHOR CONTRIBUTIONS
RPconceivedthisstudyRPandRJFraisedthegrantsforfieldworkRPBALRJFandHBdesignedthemethodologyRPcollectedthedataandperformedallstatisticalanalysesRPandFHledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandprovidedfinalapprovalforpublication
DATA ACCE SSIBILIT Y
DatacanbeaccessedthroughtheDryadDigitalRepositoryhttpsdoiorg105061dryaddk4t694 (Pillay Hua Loiselle Bernard ampFletcher2018)
ORCID
Rajeev Pillay httporcidorg0000-0002-7116-6855
R E FE R E N C E S
AshtonP (1998)Dryobalanops lanceolatahttpwwwiucnredlistorgdetails331640(accessed11March2015)
Asner G P Rudel T K Aide T M Defries R amp Emerson R(2009) A contemporary assessment of change in humid trop-ical forests Conservation Biology 23 1386ndash1395 httpsdoiorg101111j1523-1739200901333x
BagchiRGalleryREGripenbergSGurrSJNarayanLAddisCEhellipLewisOT(2014)Pathogensandinsectherbivoresdriverain-forestplantdiversityandcompositionNature50685ndash88httpsdoiorg101038nature12911
Bagchi R Philipson C D Slade E M Hector A Phillips SVillanueva J F hellip Press M C (2011) Impacts of logging ondensity-dependentpredationofdipterocarpseedsinaSouthEastAsian rainforestPhilosophical Transactions of the Royal Society B Biological Sciences 366 3246ndash3255 httpsdoiorg101098rstb20110034
Bartoń K (2016) MuMIn Multi-model inference R package version 1156
BatesDMaumlchlerMBolkerBMampWalkerSC(2015)Fittinglinearmixed-effectsmodelsusing lme4Journal of Statistical Software67httpsdoiorg1018637jssv067i01
BlundellAGampPeartDR(2004)Density-dependentpopulationdy-namicsofadominantrainforestcanopytreeEcology85704ndash715httpsdoiorg10189001-4101
BornJBagchiRBurslemDNilusRTellenbachCPluessARampGhazoulJ(2015)DifferentialresponsesofdipterocarpseedlingstosoilmoistureandmicrotopographyBiotropica4749ndash58httpsdoiorg101111btp12180
BrunaEM (1999) Seedgermination in rainforest fragmentsNature402139httpsdoiorg10103845963
BurnhamKPampAndersonDR(2002)Model Selection and Multimodel Inference A Practical Information-Theoretic ApproachNewYorkNYSpringer-Verlaghttpsdoiorg101007b97636
Caughlin T T Ferguson J M Lichstein J W Zuidema P ABunyavejchewinSampLeveyD J (2015)Lossofanimal seeddis-persalincreasesextinctionriskinatropicaltreespeciesduetoper-vasivenegativedensitydependenceacross life stagesProceedings of the Royal Society B Biological Sciences28220142095httpsdoiorg101098rspb20142095
ChambersJCampMacMahonJA (1994)Adayinthe lifeofaseedMovementsandfatesofseedsandtheirimplicationsfornaturaland
emspensp emsp | emsp8241PILLAY et AL
managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
emspensp emsp | emsp8237PILLAY et AL
32emsp|emspImpact of logging on the predation of seeds and seedlings
Over3monthswerecordedanoverallseedandseedlingpredationrate of 866 and 836 in unlogged (n=1423 seeds 140 naturalplots)andlogged(n=646seeds120naturalplots)forestrespec-tivelyAsmallnumberofseeds(unloggedforest5loggedforest8)diedofdesiccationConsistentwithprediction2therewasashiftinthefunctionalroleofseedpredatorsawayfromnon-vertebratesto-wardvertebratesinloggedforest(Figure4ab)Inthenaturalplotsthe log odds of a seedseedling being depredated by vertebrates(relativetonon-vertebrates)werehigherinloggedforestthaninun-loggedforest(βlogged079SE05095CIminus028to185Figure4aSupportinginformationTableS4)Furthersupportingprediction2the logoddsofseedandseedlingpredationwere lower intheex-perimentalexclosureplotsthaninthecontrolplotsinloggedforest(βlogged-exclosureminus210SE05795CIminus343 tominus097Figure4b)In contrast the effect of exclosure treatments on seed predationtendedtobeweakerinunloggedforest(βunlogged-exclosureminus102SE 08895CIminus290to089Figure4bSupportinginformationTableS5)
33emsp|emspImpact of logging on density- dependent germination and seedling survival
We monitored the germination and survival status of seeds thatwerealiveinthenaturalplotsatthefirstcensus(603and227seedsin unlogged and logged forest respectively) until the end of thestudy The sixmost parsimoniousmodelswith a cumulativeAICcweightof97(SupportinginformationTableS6)indicatedthatfor-est type conspecific seed density distance from the parent treeseedfall tree size canopy cover and interactions between foresttypeandtheothervariableshadsupport inexplainingvariation inseedgerminationSeedsfacedgreaterhazard(iehigherprobabilityofmortality) inloggedforestthaninunloggedforest(Table1b)as471ofseedsfailedtogerminateinloggedforestcomparedwith08 in unlogged forestHigher conspecific seed densitywas as-sociatedwithlowerseedmortalityinunloggedforestandthisrela-tionshipalsotendedtoapplyinloggedforest(Figure5aTable1b)With increasingdistancefromparenttreesseedmortalitytendedto increase in both forest types but this relationshipwasweakerin logged forest (Figure5b Table1b) Higher seedfall and largertreesizetendedtobeassociatedwithlowerseedmortalityinbothforest types (Figure5cdTable1b)With increasing canopy coverseedmortality tended to increase inboth forest types (Figure5eTable1b)
Forexplainingvariationinseedlingsurvivalthetwomostparsi-moniousmodelswithacumulativeAICcweightof99(SupportinginformationTableS7) indicated that forest type conspecific seeddensity distance from the parent tree seedfall tree size canopycoverandinteractionsbetweenforesttypeandtheothervariableshad support Of the seeds that germinated seedlings tended tohavelowerprobabilityofmortalityinloggedforestthaninunlogged
forest(Table1c)as817ofgerminatedseedlingssurviveduptotheendofthestudyinloggedforestcomparedwith311inunloggedforestHigherconspecificseedlingdensitytendedtobeassociatedwithhigherseedlingmortality inunloggedforestbut inconsistentwith prediction 3 this relationship was reversed in logged forest(Figure5f Table1c) With increasing distance from parent treesseedlingmortalityincreasedinunloggedforestbutthisrelationshiptendedtobereversedinloggedforest(Figure5gTable1c)Higherseedfall tended tobe associatedwithhigher seedlingmortality inunloggedforestbutthisrelationshipalsotendedtobereversedinloggedforest(Figure5hTable1c)Likegerminationlargertreesizetendedtobeassociatedwithlowerseedlingmortalityinbothforesttypesandthisrelationshipwasstrongerinloggedforest(Figure5iTable1c)With increasingcanopycoverseedlingmortalitytendedtoincreaseinunloggedforestbutthisrelationshiptendedtobere-versedinloggedforest(Figure5jTable1c)
4emsp |emspDISCUSSION
Ourresultsdemonstratehowmultiplestagesoftheseedlingrecruit-mentprocessofacanopytreespeciesmaybealteredwhentropicalforestsaredegradedbyintensiveldquoselectiverdquologgingConsistentwithourpredictions the remaining reproductive trees in logged forestproducedamarkedlysmallerseedcropthanthetreesinunloggedforestevenafteraccountingfortreesizeandthefunctionalroleofvertebratesinseedpredationincreasedinloggedforestwhilethatof non-vertebrates declined The strength of density-dependencein dipterocarpsmay change frompositive to negative at differentlife stages (Blundell amp Peart 2004 Curran ampWebb 2000) Thisappearedtobethecase inunloggedforestwheregermination in-creasedwithlocal-scaleconspecificseeddensitypossiblybecausepredatorsweresatiatedbythehighmast-fruitingseeddensitiesbutseedlingsurvivaltendedtodecline(Figure5afTable1bc)HoweverinconsistentwithourpredictionofstrongerNDDinloggedforestgermination and especially seedling survival increasedwith local-scaleconspecificseeddensitywhichsuggeststhatloggingmayhaveaffectedpredator-mediatedNDDduringtheseed-to-seedlingtran-sitionbottleneck inD lanceolata Importantlyourfindingsappliedtoamast-fruitingyearwhenmostdipterocarprecruitmentoccurs(CurranampLeighton2000Janzen1974)suggestingthat intensiveloggingmaypotentiallyaffectlong-termpopulationdynamicsofD lanceolataOur findings add to knowledge of how ecological pro-cesses responsible for themaintenanceofbiodiversitymaybeaf-fectedbylogging(DarrigodosSantosampVenticinque2018Ewersetal2015Schleuningetal2011Woodcocketal2013)
Increasing edaphic and drought stress in reproducing treesin logged forest may have contributed to the reduced seed crop(Curran etal 1999 Hardwick etal 2015) The consequences ofseed limitation in logged forests for sapling and ultimately adulttree recruitment remain largelyunexploredbutmaybedetrimen-tal for long-term tree population dynamics (Caughlin etal 2015)Changes in the functional roles of non-vertebrate seed predators
8238emsp |emsp emspensp PILLAY et AL
relativetovertebratesinloggedforestmaybedrivenbynumericalchanges inpredatorabundanceacrossgroups (Ewersetal2015)The altered microclimatic conditions in logged forests are likelyhostile to populations of insect seed predators and fungal patho-gens(Ewersetal2015Hardwicketal2015)Converselylogged
forestsmayprovideincreasedresourceavailabilityforrodentseedpredatorsandthusbenefittheirpopulations(Ewersetal2015)
Theuniqueecologyofmast-fruitingandtheimpactthisphenom-enonmayhavesustainedinloggedforestmayexplainthecomplexdensity-dependent patterns of germination and seedling survival(Figure5af)On theonehand in unlogged forest predator satia-tionmayhavebeenoccurringatthehighseeddensitiesduringthemast(Janzen1970)aspotentiallysupportedbyourfindingthatger-minationtendedtoincreasewithhigherseedfall(Figure5cBagchietal2011CurranampWebb2000)Indeedmast-fruitinghasbeenhypothesizedtobeanevolutionaryresponsetodensity-dependentmortality factors allowing seeds to escape predation by satiatingseedpredators (Janzen19701974)Ontheotherhand in loggedforesttheconcentratedseeddensitiesunderspatiallyisolatedadulttreesmayallowNDDtooperate(Bagchietal2011CurranampWebb2000)Howeverourfindingsofincreasedgerminationandespeciallyseedlingsurvivalwithhigherconspecificseeddensityinloggedfor-est(Figure5afTable1bc)werecontrarytotheexpectationsunderNDDandmaybeassociatedwiththediminishedfunctionalroleofnon-vertebrate seedpredators in logged forest (Figure4)NDD isprimarily driven by host-specific insect seed predators and fungalpathogenswhichtendtoconcentrateamongthehigh-seedseedingdensitiesunderthecrownsofparenttreestherebycausinghighermortalitywhere densities are higher (Bagchi etal 2014 Connell1971 Janzen 1970) These non-vertebrate seed predators andpathogensmaybedeclining in logged forests (Ewers etal 2015)andtheirecologicalroleinmaintainingNDDmaybediminishedIncontrastthetendencyofvertebratestoforageoverlargeareasmayrender predation-relatedmortality to bemore spatially heteroge-neousrelativetoseedseedlingdensities(SwamyampTerborgh2010)
Wenotethatseedcropsizegerminationandseedlingsurvivaltendedtoincreaseforlargertreesinbothforesttypes(Figures3c5di)Thissuggeststhatselectiveloggingpracticesthatharvesttim-ber at sustainable rates and followsilviculturalpracticesdesignedtominimizedamagetotheresidualstand(Asneretal2009Martinetal2015Putzetal2012)arecriticaltopreventseedlingrecruit-mentfailure indipterocarpforestsSeedgerminationandseedlingsurvivalofD lanceolatatendstobepositivelyassociatedwithlightavailability (Itoh etal 1995) which likely explains why seed andseedling mortality tended to increase with higher canopy cover(Figure5ej)
41emsp|emspCaveats and limitations
OurstudyincludedsevenandsixD lanceolatatreesasindepend-ent experimental units in unlogged and logged forests respec-tively (cfBagchietal2011HolbrookampLoiselle2009Poulsenetal 2012) The spatially clumped distributions of most adultfruiting individuals inunlogged forestand the fewspatially scat-teredadultdipterocarpsremaininginloggedforest(ofallspeciesD lanceolata was the most abundant at seven individuals) pre-cludedadditionalreplicationatthelevelofindividualtreeswithinforesttypeThesparsenumberofadultdipterocarpsinthelogged
TABLE 1emspModelaveragedestimatesexplainingvariationin(a)seedcropsize(b)germinationand(c)seedlingsurvival(upto3monthsafterseedfall)ofD lanceolatainrelationtothepredictorvariablesthatweresupportedbyAICc-basedmodelselectioncriteria(SupportinginformationTablesS2S6S7)
Response and predictor variables Estimate (SE) 95 CI
(a)Seedcropsize
Intercept 300(029) 240ndash352
Loggedforest minus080(048) minus172ndash007
Distance minus013 (001) minus014tominus011
Loggedforesttimesdistance minus001(001) minus005ndash001
Treesize 006(014) minus018ndash060
Loggedforesttimestreesize 001(010) minus054ndash080
(b)Germination
Logged forest 468 (362) 269ndash1096
Conspecific seed density minus271 (238) minus744tominus075
Logged foresttimesconspecific seed density
265 (235) 105ndash723
Distance 003(018) minus062ndash133
Loggedforesttimesdistance minus002(016) minus134ndash091
Seedfall minus084(157) minus602ndash104
Loggedforesttimesseedfall 024(149) minus422ndash1428
Treesize minus018(098) minus639ndash329
Loggedforesttimestreesize minus014(108) minus1072ndash474
Canopycover 001(032) minus217ndash255
Loggedforesttimescanopycover 015(084) minus155ndash775
(c)Seedlingsurvival
Loggedforest minus710(403) minus1500ndash081
Conspecificseedlingdensity 030(015) minus001ndash060
Logged foresttimesconspecific seedling density
minus170 (043) minus255tominus086
Distance 015 (009) 002ndash032
Logged foresttimesdistance minus104 (067) minus231 tominus012
Seedfall 003(058) minus119ndash126
Loggedforesttimesseedfall minus203(307) minus863ndash389
Treesize minus003(096) minus206ndash199
Logged foresttimestree size minus316 (205) minus706 tominus033
Canopycover 027(028) minus024ndash087
Loggedforesttimescanopycover minus034(110) minus271to191
NotesResultsforseedcropsizerepresentcoefficients(log-scale)esti-matedwithgeneralizedlinearmixedmodelsResultsforgerminationandseedling survival represent loghazardsestimatedwithCox regressionmixed-effectssurvivalmodelsEstimatesinitalicsindicatethatthe95confidenceintervalsdidnotoverlapzerosuggestingastrongeffectofthepredictorvariableonthecorrespondingresponsevariable
emspensp emsp | emsp8239PILLAY et AL
forestisareflectionofthepopulationreductionmanytimbertreespeciesaresubjected toafter intensiveselective logging (Martinetal2015)
The variable density of adultD lanceolata trees between un-logged and logged forests may introduce confounding negativedensity-dependentneighbourhoodeffectsonseedlingrecruitment(BlundellampPeart2004StollampNewbery2005)PreviousresearchontheDipterocarpaceaesuggeststhatneighbourhoodeffectsmayoccurwhenconspecificadultsarewithin20mofeachother(StollampNewbery2005)Ourrequirementofnon-overlappingseedshad-owsbetweenfocaltreesensuredthattreeswereseparatedbyatleast40mTherelativelylargerdistancebetweenthefocaltreesinourstudycomparedwiththethresholddistanceof20matwhichneighbourhoodeffectsmayoccur(StollampNewbery2005)shouldthusservetominimizethispotentialconfoundingfactor
Inanalyzingagentsofseedandseedlingpredationwedidnotdistinguishbetweenthedifferentprocessesofseedlingpredation
andherbivoryOftheseedlingsthatwerealiveinthenaturalplotsat the end of the study 017 and 176 showed signs of leafdamagetypicalofinsectherbivory(ColeyampBarone1996)inun-loggedandloggedforestsrespectively Intheexperimentalandpairedcontrolplotsthepercentageofseedlingswithsignsofleafdamage fromherbivorywas similarly small (061and065 inunloggedand logged forest respectively)Thusobservedseed-lingherbivoryrateswerelowAlonger-termstudymayrevealal-teredseedlingherbivoryrateswithlogging(Darrigoetal2018)particularly because herbivorous insect biomass was found toincrease with logging (Ewers etal 2015) Our study examinestheeffectsofintensiveselectiveloggingontheseed-to-seedlingtransitionphaseofacanopydipterocarpHoweverour findingsmaynot represent the fateofseedlingsovera longer timespanbecause ecological changes caused by logging (eg herbivory)could continue to impact the survival of seedlings beyond theseed-to-seedlingtransitionbottleneck(Caughlinetal2015)
F IGURE 4emspTheoddsofpredationofD lanceolataseedsbyvertebratesrelativetonon-vertebratesin(a)naturalplotsand(b)experimental(vertebrateexclosures)andpairedcontrolplotsinunloggedandloggedforestErrorbarsrepresent95confidenceintervals
(a) (b)
F IGURE 5emspTherelationshipsbetweenD lanceolataseedgermination(toppanel)seedlingsurvival(bottompanel)and(af)conspecificseedseedlingdensity(bg)distancefromtheparenttree(ch)seedfall(di)treesizeand(ej)canopycoverinunloggedandloggedforests
(a) (b) (c) (d) (e)
(f) (g) (h) (i) (j)
8240emsp |emsp emspensp PILLAY et AL
WedidnotmanipulatedensityanddistanceindependentlyOuruseof seeddensity gradientsnaturally generatedby thedistancegradient can identify density-dependent patterns of seedling re-cruitment (Harms etal 2000Webbamp Peart 1999)However intheabsenceofexperimentalmanipulationofdensityanddistanceeffects independent of each other our ability to understand thecauses underlying observed patterns of density-dependence inunloggedand logged forests is limited (SwamyampTerborgh2010)Futurestudiesshouldleveragemanipulativeexperimentsforanu-ancedunderstandingof the causes underlying alteredpatterns ofseedling recruitment in the face of anthropogenic disturbances(FreckletonampLewis2006)
5emsp |emspCONCLUSION
We found that for Dryobalanops lanceolata a dipterocarp spe-ciesendangeredby thecommercial timber trade (Ashton1998)multiple stages of seedling recruitment were altered in selec-tively logged forest compared with unlogged forest during amast-fruiting year Future studies should leverage broader log-ging gradients additional species and experimental approachesover longer time frames (Bagchietal2011Martinetal2015Riuttaetal2018Struebigetal2013SwamyampTerborgh2010)to quantify the thresholds of logging intensity abovewhich theecologicalprocessofseedlingrecruitmentmayunravelWehigh-lighttheimportanceofunderstandingtheimpactsofdisturbancessuch as logging on ecological processeswhich can complementnumericalassessmentsofbiodiversitytounmaskimpactsthatmayotherwiseremainhidden
ACKNOWLEDG MENTS
We thank Yayasan Sabah BentaWawasan Sdn Bhd the SabahBiodiversity Council the Sabah Forestry Department theMaliauBasin Management Committee the State Secretary Sabah ChiefMinisterrsquosDepartmenttheMalaysianEconomicPlanningUnitandtheRoyalSocietySouthEastAsiaRainforestResearchPartnershipfor granting permits Our fieldwork was funded by grants fromthe Rufford Small Grants Foundation IDEAWild the Institute ofFoodandAgriculturalSciencesandtheTropicalConservationandDevelopmentProgramattheUniversityofFloridaWethankRyanGray andMinSheng Khoo for coordinating field logistics MainusTausong JeffryAminMohdYusufDidin (Roy)RismanAjangandMelvin Teronggoh for assistance during fieldwork Magat JaparandJeffryAminfor identifyingtreesseedsandseedlingsJeffreyHostetler forhelpwith survival analysis andEmilioBrunaTrevorCaughlin David Newbery and one anonymous reviewer for con-structivecommentsthatgreatlyimprovedthemanuscript
CONFLIC T OF INTERE S T
Nonedeclared
AUTHOR CONTRIBUTIONS
RPconceivedthisstudyRPandRJFraisedthegrantsforfieldworkRPBALRJFandHBdesignedthemethodologyRPcollectedthedataandperformedallstatisticalanalysesRPandFHledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandprovidedfinalapprovalforpublication
DATA ACCE SSIBILIT Y
DatacanbeaccessedthroughtheDryadDigitalRepositoryhttpsdoiorg105061dryaddk4t694 (Pillay Hua Loiselle Bernard ampFletcher2018)
ORCID
Rajeev Pillay httporcidorg0000-0002-7116-6855
R E FE R E N C E S
AshtonP (1998)Dryobalanops lanceolatahttpwwwiucnredlistorgdetails331640(accessed11March2015)
Asner G P Rudel T K Aide T M Defries R amp Emerson R(2009) A contemporary assessment of change in humid trop-ical forests Conservation Biology 23 1386ndash1395 httpsdoiorg101111j1523-1739200901333x
BagchiRGalleryREGripenbergSGurrSJNarayanLAddisCEhellipLewisOT(2014)Pathogensandinsectherbivoresdriverain-forestplantdiversityandcompositionNature50685ndash88httpsdoiorg101038nature12911
Bagchi R Philipson C D Slade E M Hector A Phillips SVillanueva J F hellip Press M C (2011) Impacts of logging ondensity-dependentpredationofdipterocarpseedsinaSouthEastAsian rainforestPhilosophical Transactions of the Royal Society B Biological Sciences 366 3246ndash3255 httpsdoiorg101098rstb20110034
Bartoń K (2016) MuMIn Multi-model inference R package version 1156
BatesDMaumlchlerMBolkerBMampWalkerSC(2015)Fittinglinearmixed-effectsmodelsusing lme4Journal of Statistical Software67httpsdoiorg1018637jssv067i01
BlundellAGampPeartDR(2004)Density-dependentpopulationdy-namicsofadominantrainforestcanopytreeEcology85704ndash715httpsdoiorg10189001-4101
BornJBagchiRBurslemDNilusRTellenbachCPluessARampGhazoulJ(2015)DifferentialresponsesofdipterocarpseedlingstosoilmoistureandmicrotopographyBiotropica4749ndash58httpsdoiorg101111btp12180
BrunaEM (1999) Seedgermination in rainforest fragmentsNature402139httpsdoiorg10103845963
BurnhamKPampAndersonDR(2002)Model Selection and Multimodel Inference A Practical Information-Theoretic ApproachNewYorkNYSpringer-Verlaghttpsdoiorg101007b97636
Caughlin T T Ferguson J M Lichstein J W Zuidema P ABunyavejchewinSampLeveyD J (2015)Lossofanimal seeddis-persalincreasesextinctionriskinatropicaltreespeciesduetoper-vasivenegativedensitydependenceacross life stagesProceedings of the Royal Society B Biological Sciences28220142095httpsdoiorg101098rspb20142095
ChambersJCampMacMahonJA (1994)Adayinthe lifeofaseedMovementsandfatesofseedsandtheirimplicationsfornaturaland
emspensp emsp | emsp8241PILLAY et AL
managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
8238emsp |emsp emspensp PILLAY et AL
relativetovertebratesinloggedforestmaybedrivenbynumericalchanges inpredatorabundanceacrossgroups (Ewersetal2015)The altered microclimatic conditions in logged forests are likelyhostile to populations of insect seed predators and fungal patho-gens(Ewersetal2015Hardwicketal2015)Converselylogged
forestsmayprovideincreasedresourceavailabilityforrodentseedpredatorsandthusbenefittheirpopulations(Ewersetal2015)
Theuniqueecologyofmast-fruitingandtheimpactthisphenom-enonmayhavesustainedinloggedforestmayexplainthecomplexdensity-dependent patterns of germination and seedling survival(Figure5af)On theonehand in unlogged forest predator satia-tionmayhavebeenoccurringatthehighseeddensitiesduringthemast(Janzen1970)aspotentiallysupportedbyourfindingthatger-minationtendedtoincreasewithhigherseedfall(Figure5cBagchietal2011CurranampWebb2000)Indeedmast-fruitinghasbeenhypothesizedtobeanevolutionaryresponsetodensity-dependentmortality factors allowing seeds to escape predation by satiatingseedpredators (Janzen19701974)Ontheotherhand in loggedforesttheconcentratedseeddensitiesunderspatiallyisolatedadulttreesmayallowNDDtooperate(Bagchietal2011CurranampWebb2000)Howeverourfindingsofincreasedgerminationandespeciallyseedlingsurvivalwithhigherconspecificseeddensityinloggedfor-est(Figure5afTable1bc)werecontrarytotheexpectationsunderNDDandmaybeassociatedwiththediminishedfunctionalroleofnon-vertebrate seedpredators in logged forest (Figure4)NDD isprimarily driven by host-specific insect seed predators and fungalpathogenswhichtendtoconcentrateamongthehigh-seedseedingdensitiesunderthecrownsofparenttreestherebycausinghighermortalitywhere densities are higher (Bagchi etal 2014 Connell1971 Janzen 1970) These non-vertebrate seed predators andpathogensmaybedeclining in logged forests (Ewers etal 2015)andtheirecologicalroleinmaintainingNDDmaybediminishedIncontrastthetendencyofvertebratestoforageoverlargeareasmayrender predation-relatedmortality to bemore spatially heteroge-neousrelativetoseedseedlingdensities(SwamyampTerborgh2010)
Wenotethatseedcropsizegerminationandseedlingsurvivaltendedtoincreaseforlargertreesinbothforesttypes(Figures3c5di)Thissuggeststhatselectiveloggingpracticesthatharvesttim-ber at sustainable rates and followsilviculturalpracticesdesignedtominimizedamagetotheresidualstand(Asneretal2009Martinetal2015Putzetal2012)arecriticaltopreventseedlingrecruit-mentfailure indipterocarpforestsSeedgerminationandseedlingsurvivalofD lanceolatatendstobepositivelyassociatedwithlightavailability (Itoh etal 1995) which likely explains why seed andseedling mortality tended to increase with higher canopy cover(Figure5ej)
41emsp|emspCaveats and limitations
OurstudyincludedsevenandsixD lanceolatatreesasindepend-ent experimental units in unlogged and logged forests respec-tively (cfBagchietal2011HolbrookampLoiselle2009Poulsenetal 2012) The spatially clumped distributions of most adultfruiting individuals inunlogged forestand the fewspatially scat-teredadultdipterocarpsremaininginloggedforest(ofallspeciesD lanceolata was the most abundant at seven individuals) pre-cludedadditionalreplicationatthelevelofindividualtreeswithinforesttypeThesparsenumberofadultdipterocarpsinthelogged
TABLE 1emspModelaveragedestimatesexplainingvariationin(a)seedcropsize(b)germinationand(c)seedlingsurvival(upto3monthsafterseedfall)ofD lanceolatainrelationtothepredictorvariablesthatweresupportedbyAICc-basedmodelselectioncriteria(SupportinginformationTablesS2S6S7)
Response and predictor variables Estimate (SE) 95 CI
(a)Seedcropsize
Intercept 300(029) 240ndash352
Loggedforest minus080(048) minus172ndash007
Distance minus013 (001) minus014tominus011
Loggedforesttimesdistance minus001(001) minus005ndash001
Treesize 006(014) minus018ndash060
Loggedforesttimestreesize 001(010) minus054ndash080
(b)Germination
Logged forest 468 (362) 269ndash1096
Conspecific seed density minus271 (238) minus744tominus075
Logged foresttimesconspecific seed density
265 (235) 105ndash723
Distance 003(018) minus062ndash133
Loggedforesttimesdistance minus002(016) minus134ndash091
Seedfall minus084(157) minus602ndash104
Loggedforesttimesseedfall 024(149) minus422ndash1428
Treesize minus018(098) minus639ndash329
Loggedforesttimestreesize minus014(108) minus1072ndash474
Canopycover 001(032) minus217ndash255
Loggedforesttimescanopycover 015(084) minus155ndash775
(c)Seedlingsurvival
Loggedforest minus710(403) minus1500ndash081
Conspecificseedlingdensity 030(015) minus001ndash060
Logged foresttimesconspecific seedling density
minus170 (043) minus255tominus086
Distance 015 (009) 002ndash032
Logged foresttimesdistance minus104 (067) minus231 tominus012
Seedfall 003(058) minus119ndash126
Loggedforesttimesseedfall minus203(307) minus863ndash389
Treesize minus003(096) minus206ndash199
Logged foresttimestree size minus316 (205) minus706 tominus033
Canopycover 027(028) minus024ndash087
Loggedforesttimescanopycover minus034(110) minus271to191
NotesResultsforseedcropsizerepresentcoefficients(log-scale)esti-matedwithgeneralizedlinearmixedmodelsResultsforgerminationandseedling survival represent loghazardsestimatedwithCox regressionmixed-effectssurvivalmodelsEstimatesinitalicsindicatethatthe95confidenceintervalsdidnotoverlapzerosuggestingastrongeffectofthepredictorvariableonthecorrespondingresponsevariable
emspensp emsp | emsp8239PILLAY et AL
forestisareflectionofthepopulationreductionmanytimbertreespeciesaresubjected toafter intensiveselective logging (Martinetal2015)
The variable density of adultD lanceolata trees between un-logged and logged forests may introduce confounding negativedensity-dependentneighbourhoodeffectsonseedlingrecruitment(BlundellampPeart2004StollampNewbery2005)PreviousresearchontheDipterocarpaceaesuggeststhatneighbourhoodeffectsmayoccurwhenconspecificadultsarewithin20mofeachother(StollampNewbery2005)Ourrequirementofnon-overlappingseedshad-owsbetweenfocaltreesensuredthattreeswereseparatedbyatleast40mTherelativelylargerdistancebetweenthefocaltreesinourstudycomparedwiththethresholddistanceof20matwhichneighbourhoodeffectsmayoccur(StollampNewbery2005)shouldthusservetominimizethispotentialconfoundingfactor
Inanalyzingagentsofseedandseedlingpredationwedidnotdistinguishbetweenthedifferentprocessesofseedlingpredation
andherbivoryOftheseedlingsthatwerealiveinthenaturalplotsat the end of the study 017 and 176 showed signs of leafdamagetypicalofinsectherbivory(ColeyampBarone1996)inun-loggedandloggedforestsrespectively Intheexperimentalandpairedcontrolplotsthepercentageofseedlingswithsignsofleafdamage fromherbivorywas similarly small (061and065 inunloggedand logged forest respectively)Thusobservedseed-lingherbivoryrateswerelowAlonger-termstudymayrevealal-teredseedlingherbivoryrateswithlogging(Darrigoetal2018)particularly because herbivorous insect biomass was found toincrease with logging (Ewers etal 2015) Our study examinestheeffectsofintensiveselectiveloggingontheseed-to-seedlingtransitionphaseofacanopydipterocarpHoweverour findingsmaynot represent the fateofseedlingsovera longer timespanbecause ecological changes caused by logging (eg herbivory)could continue to impact the survival of seedlings beyond theseed-to-seedlingtransitionbottleneck(Caughlinetal2015)
F IGURE 4emspTheoddsofpredationofD lanceolataseedsbyvertebratesrelativetonon-vertebratesin(a)naturalplotsand(b)experimental(vertebrateexclosures)andpairedcontrolplotsinunloggedandloggedforestErrorbarsrepresent95confidenceintervals
(a) (b)
F IGURE 5emspTherelationshipsbetweenD lanceolataseedgermination(toppanel)seedlingsurvival(bottompanel)and(af)conspecificseedseedlingdensity(bg)distancefromtheparenttree(ch)seedfall(di)treesizeand(ej)canopycoverinunloggedandloggedforests
(a) (b) (c) (d) (e)
(f) (g) (h) (i) (j)
8240emsp |emsp emspensp PILLAY et AL
WedidnotmanipulatedensityanddistanceindependentlyOuruseof seeddensity gradientsnaturally generatedby thedistancegradient can identify density-dependent patterns of seedling re-cruitment (Harms etal 2000Webbamp Peart 1999)However intheabsenceofexperimentalmanipulationofdensityanddistanceeffects independent of each other our ability to understand thecauses underlying observed patterns of density-dependence inunloggedand logged forests is limited (SwamyampTerborgh2010)Futurestudiesshouldleveragemanipulativeexperimentsforanu-ancedunderstandingof the causes underlying alteredpatterns ofseedling recruitment in the face of anthropogenic disturbances(FreckletonampLewis2006)
5emsp |emspCONCLUSION
We found that for Dryobalanops lanceolata a dipterocarp spe-ciesendangeredby thecommercial timber trade (Ashton1998)multiple stages of seedling recruitment were altered in selec-tively logged forest compared with unlogged forest during amast-fruiting year Future studies should leverage broader log-ging gradients additional species and experimental approachesover longer time frames (Bagchietal2011Martinetal2015Riuttaetal2018Struebigetal2013SwamyampTerborgh2010)to quantify the thresholds of logging intensity abovewhich theecologicalprocessofseedlingrecruitmentmayunravelWehigh-lighttheimportanceofunderstandingtheimpactsofdisturbancessuch as logging on ecological processeswhich can complementnumericalassessmentsofbiodiversitytounmaskimpactsthatmayotherwiseremainhidden
ACKNOWLEDG MENTS
We thank Yayasan Sabah BentaWawasan Sdn Bhd the SabahBiodiversity Council the Sabah Forestry Department theMaliauBasin Management Committee the State Secretary Sabah ChiefMinisterrsquosDepartmenttheMalaysianEconomicPlanningUnitandtheRoyalSocietySouthEastAsiaRainforestResearchPartnershipfor granting permits Our fieldwork was funded by grants fromthe Rufford Small Grants Foundation IDEAWild the Institute ofFoodandAgriculturalSciencesandtheTropicalConservationandDevelopmentProgramattheUniversityofFloridaWethankRyanGray andMinSheng Khoo for coordinating field logistics MainusTausong JeffryAminMohdYusufDidin (Roy)RismanAjangandMelvin Teronggoh for assistance during fieldwork Magat JaparandJeffryAminfor identifyingtreesseedsandseedlingsJeffreyHostetler forhelpwith survival analysis andEmilioBrunaTrevorCaughlin David Newbery and one anonymous reviewer for con-structivecommentsthatgreatlyimprovedthemanuscript
CONFLIC T OF INTERE S T
Nonedeclared
AUTHOR CONTRIBUTIONS
RPconceivedthisstudyRPandRJFraisedthegrantsforfieldworkRPBALRJFandHBdesignedthemethodologyRPcollectedthedataandperformedallstatisticalanalysesRPandFHledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandprovidedfinalapprovalforpublication
DATA ACCE SSIBILIT Y
DatacanbeaccessedthroughtheDryadDigitalRepositoryhttpsdoiorg105061dryaddk4t694 (Pillay Hua Loiselle Bernard ampFletcher2018)
ORCID
Rajeev Pillay httporcidorg0000-0002-7116-6855
R E FE R E N C E S
AshtonP (1998)Dryobalanops lanceolatahttpwwwiucnredlistorgdetails331640(accessed11March2015)
Asner G P Rudel T K Aide T M Defries R amp Emerson R(2009) A contemporary assessment of change in humid trop-ical forests Conservation Biology 23 1386ndash1395 httpsdoiorg101111j1523-1739200901333x
BagchiRGalleryREGripenbergSGurrSJNarayanLAddisCEhellipLewisOT(2014)Pathogensandinsectherbivoresdriverain-forestplantdiversityandcompositionNature50685ndash88httpsdoiorg101038nature12911
Bagchi R Philipson C D Slade E M Hector A Phillips SVillanueva J F hellip Press M C (2011) Impacts of logging ondensity-dependentpredationofdipterocarpseedsinaSouthEastAsian rainforestPhilosophical Transactions of the Royal Society B Biological Sciences 366 3246ndash3255 httpsdoiorg101098rstb20110034
Bartoń K (2016) MuMIn Multi-model inference R package version 1156
BatesDMaumlchlerMBolkerBMampWalkerSC(2015)Fittinglinearmixed-effectsmodelsusing lme4Journal of Statistical Software67httpsdoiorg1018637jssv067i01
BlundellAGampPeartDR(2004)Density-dependentpopulationdy-namicsofadominantrainforestcanopytreeEcology85704ndash715httpsdoiorg10189001-4101
BornJBagchiRBurslemDNilusRTellenbachCPluessARampGhazoulJ(2015)DifferentialresponsesofdipterocarpseedlingstosoilmoistureandmicrotopographyBiotropica4749ndash58httpsdoiorg101111btp12180
BrunaEM (1999) Seedgermination in rainforest fragmentsNature402139httpsdoiorg10103845963
BurnhamKPampAndersonDR(2002)Model Selection and Multimodel Inference A Practical Information-Theoretic ApproachNewYorkNYSpringer-Verlaghttpsdoiorg101007b97636
Caughlin T T Ferguson J M Lichstein J W Zuidema P ABunyavejchewinSampLeveyD J (2015)Lossofanimal seeddis-persalincreasesextinctionriskinatropicaltreespeciesduetoper-vasivenegativedensitydependenceacross life stagesProceedings of the Royal Society B Biological Sciences28220142095httpsdoiorg101098rspb20142095
ChambersJCampMacMahonJA (1994)Adayinthe lifeofaseedMovementsandfatesofseedsandtheirimplicationsfornaturaland
emspensp emsp | emsp8241PILLAY et AL
managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
emspensp emsp | emsp8239PILLAY et AL
forestisareflectionofthepopulationreductionmanytimbertreespeciesaresubjected toafter intensiveselective logging (Martinetal2015)
The variable density of adultD lanceolata trees between un-logged and logged forests may introduce confounding negativedensity-dependentneighbourhoodeffectsonseedlingrecruitment(BlundellampPeart2004StollampNewbery2005)PreviousresearchontheDipterocarpaceaesuggeststhatneighbourhoodeffectsmayoccurwhenconspecificadultsarewithin20mofeachother(StollampNewbery2005)Ourrequirementofnon-overlappingseedshad-owsbetweenfocaltreesensuredthattreeswereseparatedbyatleast40mTherelativelylargerdistancebetweenthefocaltreesinourstudycomparedwiththethresholddistanceof20matwhichneighbourhoodeffectsmayoccur(StollampNewbery2005)shouldthusservetominimizethispotentialconfoundingfactor
Inanalyzingagentsofseedandseedlingpredationwedidnotdistinguishbetweenthedifferentprocessesofseedlingpredation
andherbivoryOftheseedlingsthatwerealiveinthenaturalplotsat the end of the study 017 and 176 showed signs of leafdamagetypicalofinsectherbivory(ColeyampBarone1996)inun-loggedandloggedforestsrespectively Intheexperimentalandpairedcontrolplotsthepercentageofseedlingswithsignsofleafdamage fromherbivorywas similarly small (061and065 inunloggedand logged forest respectively)Thusobservedseed-lingherbivoryrateswerelowAlonger-termstudymayrevealal-teredseedlingherbivoryrateswithlogging(Darrigoetal2018)particularly because herbivorous insect biomass was found toincrease with logging (Ewers etal 2015) Our study examinestheeffectsofintensiveselectiveloggingontheseed-to-seedlingtransitionphaseofacanopydipterocarpHoweverour findingsmaynot represent the fateofseedlingsovera longer timespanbecause ecological changes caused by logging (eg herbivory)could continue to impact the survival of seedlings beyond theseed-to-seedlingtransitionbottleneck(Caughlinetal2015)
F IGURE 4emspTheoddsofpredationofD lanceolataseedsbyvertebratesrelativetonon-vertebratesin(a)naturalplotsand(b)experimental(vertebrateexclosures)andpairedcontrolplotsinunloggedandloggedforestErrorbarsrepresent95confidenceintervals
(a) (b)
F IGURE 5emspTherelationshipsbetweenD lanceolataseedgermination(toppanel)seedlingsurvival(bottompanel)and(af)conspecificseedseedlingdensity(bg)distancefromtheparenttree(ch)seedfall(di)treesizeand(ej)canopycoverinunloggedandloggedforests
(a) (b) (c) (d) (e)
(f) (g) (h) (i) (j)
8240emsp |emsp emspensp PILLAY et AL
WedidnotmanipulatedensityanddistanceindependentlyOuruseof seeddensity gradientsnaturally generatedby thedistancegradient can identify density-dependent patterns of seedling re-cruitment (Harms etal 2000Webbamp Peart 1999)However intheabsenceofexperimentalmanipulationofdensityanddistanceeffects independent of each other our ability to understand thecauses underlying observed patterns of density-dependence inunloggedand logged forests is limited (SwamyampTerborgh2010)Futurestudiesshouldleveragemanipulativeexperimentsforanu-ancedunderstandingof the causes underlying alteredpatterns ofseedling recruitment in the face of anthropogenic disturbances(FreckletonampLewis2006)
5emsp |emspCONCLUSION
We found that for Dryobalanops lanceolata a dipterocarp spe-ciesendangeredby thecommercial timber trade (Ashton1998)multiple stages of seedling recruitment were altered in selec-tively logged forest compared with unlogged forest during amast-fruiting year Future studies should leverage broader log-ging gradients additional species and experimental approachesover longer time frames (Bagchietal2011Martinetal2015Riuttaetal2018Struebigetal2013SwamyampTerborgh2010)to quantify the thresholds of logging intensity abovewhich theecologicalprocessofseedlingrecruitmentmayunravelWehigh-lighttheimportanceofunderstandingtheimpactsofdisturbancessuch as logging on ecological processeswhich can complementnumericalassessmentsofbiodiversitytounmaskimpactsthatmayotherwiseremainhidden
ACKNOWLEDG MENTS
We thank Yayasan Sabah BentaWawasan Sdn Bhd the SabahBiodiversity Council the Sabah Forestry Department theMaliauBasin Management Committee the State Secretary Sabah ChiefMinisterrsquosDepartmenttheMalaysianEconomicPlanningUnitandtheRoyalSocietySouthEastAsiaRainforestResearchPartnershipfor granting permits Our fieldwork was funded by grants fromthe Rufford Small Grants Foundation IDEAWild the Institute ofFoodandAgriculturalSciencesandtheTropicalConservationandDevelopmentProgramattheUniversityofFloridaWethankRyanGray andMinSheng Khoo for coordinating field logistics MainusTausong JeffryAminMohdYusufDidin (Roy)RismanAjangandMelvin Teronggoh for assistance during fieldwork Magat JaparandJeffryAminfor identifyingtreesseedsandseedlingsJeffreyHostetler forhelpwith survival analysis andEmilioBrunaTrevorCaughlin David Newbery and one anonymous reviewer for con-structivecommentsthatgreatlyimprovedthemanuscript
CONFLIC T OF INTERE S T
Nonedeclared
AUTHOR CONTRIBUTIONS
RPconceivedthisstudyRPandRJFraisedthegrantsforfieldworkRPBALRJFandHBdesignedthemethodologyRPcollectedthedataandperformedallstatisticalanalysesRPandFHledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandprovidedfinalapprovalforpublication
DATA ACCE SSIBILIT Y
DatacanbeaccessedthroughtheDryadDigitalRepositoryhttpsdoiorg105061dryaddk4t694 (Pillay Hua Loiselle Bernard ampFletcher2018)
ORCID
Rajeev Pillay httporcidorg0000-0002-7116-6855
R E FE R E N C E S
AshtonP (1998)Dryobalanops lanceolatahttpwwwiucnredlistorgdetails331640(accessed11March2015)
Asner G P Rudel T K Aide T M Defries R amp Emerson R(2009) A contemporary assessment of change in humid trop-ical forests Conservation Biology 23 1386ndash1395 httpsdoiorg101111j1523-1739200901333x
BagchiRGalleryREGripenbergSGurrSJNarayanLAddisCEhellipLewisOT(2014)Pathogensandinsectherbivoresdriverain-forestplantdiversityandcompositionNature50685ndash88httpsdoiorg101038nature12911
Bagchi R Philipson C D Slade E M Hector A Phillips SVillanueva J F hellip Press M C (2011) Impacts of logging ondensity-dependentpredationofdipterocarpseedsinaSouthEastAsian rainforestPhilosophical Transactions of the Royal Society B Biological Sciences 366 3246ndash3255 httpsdoiorg101098rstb20110034
Bartoń K (2016) MuMIn Multi-model inference R package version 1156
BatesDMaumlchlerMBolkerBMampWalkerSC(2015)Fittinglinearmixed-effectsmodelsusing lme4Journal of Statistical Software67httpsdoiorg1018637jssv067i01
BlundellAGampPeartDR(2004)Density-dependentpopulationdy-namicsofadominantrainforestcanopytreeEcology85704ndash715httpsdoiorg10189001-4101
BornJBagchiRBurslemDNilusRTellenbachCPluessARampGhazoulJ(2015)DifferentialresponsesofdipterocarpseedlingstosoilmoistureandmicrotopographyBiotropica4749ndash58httpsdoiorg101111btp12180
BrunaEM (1999) Seedgermination in rainforest fragmentsNature402139httpsdoiorg10103845963
BurnhamKPampAndersonDR(2002)Model Selection and Multimodel Inference A Practical Information-Theoretic ApproachNewYorkNYSpringer-Verlaghttpsdoiorg101007b97636
Caughlin T T Ferguson J M Lichstein J W Zuidema P ABunyavejchewinSampLeveyD J (2015)Lossofanimal seeddis-persalincreasesextinctionriskinatropicaltreespeciesduetoper-vasivenegativedensitydependenceacross life stagesProceedings of the Royal Society B Biological Sciences28220142095httpsdoiorg101098rspb20142095
ChambersJCampMacMahonJA (1994)Adayinthe lifeofaseedMovementsandfatesofseedsandtheirimplicationsfornaturaland
emspensp emsp | emsp8241PILLAY et AL
managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
8240emsp |emsp emspensp PILLAY et AL
WedidnotmanipulatedensityanddistanceindependentlyOuruseof seeddensity gradientsnaturally generatedby thedistancegradient can identify density-dependent patterns of seedling re-cruitment (Harms etal 2000Webbamp Peart 1999)However intheabsenceofexperimentalmanipulationofdensityanddistanceeffects independent of each other our ability to understand thecauses underlying observed patterns of density-dependence inunloggedand logged forests is limited (SwamyampTerborgh2010)Futurestudiesshouldleveragemanipulativeexperimentsforanu-ancedunderstandingof the causes underlying alteredpatterns ofseedling recruitment in the face of anthropogenic disturbances(FreckletonampLewis2006)
5emsp |emspCONCLUSION
We found that for Dryobalanops lanceolata a dipterocarp spe-ciesendangeredby thecommercial timber trade (Ashton1998)multiple stages of seedling recruitment were altered in selec-tively logged forest compared with unlogged forest during amast-fruiting year Future studies should leverage broader log-ging gradients additional species and experimental approachesover longer time frames (Bagchietal2011Martinetal2015Riuttaetal2018Struebigetal2013SwamyampTerborgh2010)to quantify the thresholds of logging intensity abovewhich theecologicalprocessofseedlingrecruitmentmayunravelWehigh-lighttheimportanceofunderstandingtheimpactsofdisturbancessuch as logging on ecological processeswhich can complementnumericalassessmentsofbiodiversitytounmaskimpactsthatmayotherwiseremainhidden
ACKNOWLEDG MENTS
We thank Yayasan Sabah BentaWawasan Sdn Bhd the SabahBiodiversity Council the Sabah Forestry Department theMaliauBasin Management Committee the State Secretary Sabah ChiefMinisterrsquosDepartmenttheMalaysianEconomicPlanningUnitandtheRoyalSocietySouthEastAsiaRainforestResearchPartnershipfor granting permits Our fieldwork was funded by grants fromthe Rufford Small Grants Foundation IDEAWild the Institute ofFoodandAgriculturalSciencesandtheTropicalConservationandDevelopmentProgramattheUniversityofFloridaWethankRyanGray andMinSheng Khoo for coordinating field logistics MainusTausong JeffryAminMohdYusufDidin (Roy)RismanAjangandMelvin Teronggoh for assistance during fieldwork Magat JaparandJeffryAminfor identifyingtreesseedsandseedlingsJeffreyHostetler forhelpwith survival analysis andEmilioBrunaTrevorCaughlin David Newbery and one anonymous reviewer for con-structivecommentsthatgreatlyimprovedthemanuscript
CONFLIC T OF INTERE S T
Nonedeclared
AUTHOR CONTRIBUTIONS
RPconceivedthisstudyRPandRJFraisedthegrantsforfieldworkRPBALRJFandHBdesignedthemethodologyRPcollectedthedataandperformedallstatisticalanalysesRPandFHledthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandprovidedfinalapprovalforpublication
DATA ACCE SSIBILIT Y
DatacanbeaccessedthroughtheDryadDigitalRepositoryhttpsdoiorg105061dryaddk4t694 (Pillay Hua Loiselle Bernard ampFletcher2018)
ORCID
Rajeev Pillay httporcidorg0000-0002-7116-6855
R E FE R E N C E S
AshtonP (1998)Dryobalanops lanceolatahttpwwwiucnredlistorgdetails331640(accessed11March2015)
Asner G P Rudel T K Aide T M Defries R amp Emerson R(2009) A contemporary assessment of change in humid trop-ical forests Conservation Biology 23 1386ndash1395 httpsdoiorg101111j1523-1739200901333x
BagchiRGalleryREGripenbergSGurrSJNarayanLAddisCEhellipLewisOT(2014)Pathogensandinsectherbivoresdriverain-forestplantdiversityandcompositionNature50685ndash88httpsdoiorg101038nature12911
Bagchi R Philipson C D Slade E M Hector A Phillips SVillanueva J F hellip Press M C (2011) Impacts of logging ondensity-dependentpredationofdipterocarpseedsinaSouthEastAsian rainforestPhilosophical Transactions of the Royal Society B Biological Sciences 366 3246ndash3255 httpsdoiorg101098rstb20110034
Bartoń K (2016) MuMIn Multi-model inference R package version 1156
BatesDMaumlchlerMBolkerBMampWalkerSC(2015)Fittinglinearmixed-effectsmodelsusing lme4Journal of Statistical Software67httpsdoiorg1018637jssv067i01
BlundellAGampPeartDR(2004)Density-dependentpopulationdy-namicsofadominantrainforestcanopytreeEcology85704ndash715httpsdoiorg10189001-4101
BornJBagchiRBurslemDNilusRTellenbachCPluessARampGhazoulJ(2015)DifferentialresponsesofdipterocarpseedlingstosoilmoistureandmicrotopographyBiotropica4749ndash58httpsdoiorg101111btp12180
BrunaEM (1999) Seedgermination in rainforest fragmentsNature402139httpsdoiorg10103845963
BurnhamKPampAndersonDR(2002)Model Selection and Multimodel Inference A Practical Information-Theoretic ApproachNewYorkNYSpringer-Verlaghttpsdoiorg101007b97636
Caughlin T T Ferguson J M Lichstein J W Zuidema P ABunyavejchewinSampLeveyD J (2015)Lossofanimal seeddis-persalincreasesextinctionriskinatropicaltreespeciesduetoper-vasivenegativedensitydependenceacross life stagesProceedings of the Royal Society B Biological Sciences28220142095httpsdoiorg101098rspb20142095
ChambersJCampMacMahonJA (1994)Adayinthe lifeofaseedMovementsandfatesofseedsandtheirimplicationsfornaturaland
emspensp emsp | emsp8241PILLAY et AL
managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
emspensp emsp | emsp8241PILLAY et AL
managedsystemsAnnual Review of Ecology and Systematics25263ndash292httpsdoiorg101146annureves25110194001403
Chazdon R L (2003) Tropical forest recovery Legacies ofhuman impact and natural disturbances Perspectives in Plant Ecology Evolution and Systematics 6 51ndash71 httpsdoiorg1010781433-8319-00042
Chesson P (2000) Mechanisms of maintenance of species diversityAnnual Review of Ecology and Systematics31343ndash366httpsdoiorg101146annurevecolsys311343
Chong B SH (2005) Special Environmental Impact Assessment (SEIA) for the Proposed Oil Palm Plantation and Industrial Tree Plantation Development at Benta Wawasan I and Benta Wawasan IIC Yayasan Sabah Forest Management Area Kalabakan and Gunung Rara Forest Reserves TawauKotaKinabaluSabahMalaysia
ColeyPDampBaroneJA(1996)Herbivoryandplantdefensesintrop-icalforestsAnnual Review of Ecology and Systematics27305ndash335httpsdoiorg101146annurevecolsys271305
ComitaLSMuller-LandauHCAguilarSampHubbellSP (2010)Asymmetric density dependence shapes species abundances ina tropical tree community Science 329 330ndash332 httpsdoiorg101126science1190772
Connell J H (1971) On the role of natural enemies in preventingcompetitive exclusion in somemarine animals and in rain foresttreesInPJdenBoerampGRGradwell (Eds)Dynamics of num-bers in populations (pp298ndash312)WageningenTheNetherlandsPUDOC
CousensRDythamCampLawR (2008)Dispersal in plants A popu-lation perspectiveOxfordUKOxfordUniversityPresshttpsdoiorg101093acprofoso97801992991260010001
CurranLMCaniagoIPaoliGDAstianiDKusnetiMLeightonMhellipHaerumanH(1999)ImpactofElNintildeoandloggingoncanopytree recruitment in Borneo Science 286 2184ndash2188 httpsdoiorg101126science28654472184
CurranLMampLeightonM(2000)Vertebrateresponsestospatiotem-poralvariationinseedproductionofmast-fruitingDipterocarpaceaeEcological Monographs70101ndash128httpsdoiorg1018900012-9615(2000)070[0101VRTSVI]20CO2
Curran L M amp Webb C O (2000) Experimental tests of thespatiotemporal scale of seed predation in mast-fruitingDipterocarpaceaeEcological Monographs70129ndash148httpsdoiorg1018900012-9615(2000)070[0129ETOTSS]20CO2
DarrigoMRdosSantosFAMampVenticinqueEM(2018)Thecon-foundingeffectsof loggingontreeseedlinggrowthandherbivoryinCentralAmazonBiotropica50 60ndash68httpsdoiorg101111btp12483
EdwardsD P Tobias J A SheilDMeijaard E amp LauranceW F(2014)Maintainingecosystemfunctionandservicesinloggedtrop-icalforestsTrends in Ecology and Evolution29511ndash520httpsdoiorg101016jtree201407003
EwersRMDidhamRKFahrigLFerrazGHectorAHoltRDhellipTurnerEC(2011)Alarge-scaleforestfragmentationexperimentThe stability of altered forest ecosystems project Philosophical Transactions of the Royal Society B Biological Sciences 366 3292ndash3302httpsdoiorg101098rstb20110049
EwersRMBoyleMJGleaveRAPlowmanNSBenedickSBernardHhellipTurnerEC(2015)Loggingcutsthefunctionalimpor-tanceofinvertebratesintropicalrainforestNature Communications66836httpsdoiorg101038ncomms7836
Fisher B Edwards D P Larsen T H Ansell F A Hsu W WRoberts C S amp Wilcove D S (2011) Cost-effective con-servation Calculating biodiversity and logging trade-offs inSoutheast Asia Conservation Letters 4 443ndash450 httpsdoiorg101111j1755-263X201100198x
FreckletonRPampLewisOT(2006)PathogensdensitydependenceandthecoexistenceoftropicaltreesProceedings of the Royal Society
B Biological Sciences 273 2909ndash2916 httpsdoiorg101098rspb20063660
Ghazoul JListonKAampBoyleT JB (1998)Disturbance induceddensity-dependentseedsetinShorea siamensis(Dipterocarpaceae)a tropical forest tree Journal of Ecology86 462ndash473 httpsdoiorg101046j1365-2745199800270x
HardwickSRToumiRPfeiferMTurnerECNilusRampEwersRM(2015)TherelationshipbetweenleafareaindexandmicroclimateintropicalforestandoilpalmplantationForestdisturbancedriveschanges in microclimate Agricultural and Forest Meteorology 201187ndash195httpsdoiorg101016jagrformet201411010
HarmsKEWrightSJCalderoacutenOHernaacutendezAampHerreEA(2000) Pervasive density-dependent recruitment enhances seed-lingdiversityinatropicalforestNature404493ndash495httpsdoiorg10103835006630
Holbrook K M amp Loiselle B A (2009) Dispersal in a Neotropicaltree Virola flexuosa (Myristicaceae) Does hunting of large ver-tebrates limit seed removal Ecology 90 1449ndash1455 httpsdoiorg10189008-13321
ItohAYamakuraTOginoKampLeeHS (1995)Survivorshipandgrowth of seedlings of four dipterocarp species in a tropical rain-forestofSarawakEastMalaysiaEcological Research10327ndash338httpsdoiorg101007BF02347859
ItohAYamakuraTOginoKLeeHSampAshtonPS(1997)SpatialdistributionpatternsoftwopredominantemergenttreesinatropicalrainforestinSarawakMalaysiaPlant Ecology132121ndash136httpsdoiorg101023A1009779424279
Janzen D H (1970) Herbivores and the number of tree species intropicalforestsThe American Naturalist104501ndash528httpsdoiorg101086282687
Janzen D H (1974) Tropical blackwater rivers animals and mastfruitingby thedipterocarpaceaeBiotropica669ndash103httpsdoiorg1023072989823
KobeRK(1999)LightgradientpartitioningamongtropicaltreespeciesthroughseedlingmortalityampgrowthEcology80187ndash201httpsdoiorg1018900012-9658(1999)080[0187LGPATT]20CO2
LewisOTampGripenbergS(2008)Insectseedpredatorsandenviron-mentalchangeJournal of Applied Ecology451593ndash1599httpsdoiorg101111j1365-2664200801575x
MartinPANewtonACPfeiferMKhooMampBullockJM(2015)Impactsoftropicalselectiveloggingoncarbonstorageandtreespe-ciesrichnessAmeta-analysisForest Ecology and Management356224ndash233httpsdoiorg101016jforeco201507010
MurawskiDANimalGunatilleke IAUampBawaKS (1994)Theeffects of selective logging on inbreeding in Shorea megistophylla (Dipterocarpaceae) from Sri Lanka Conservation Biology 8 997ndash1002httpsdoiorg101046j1523-1739199408040997x
NorghauerJMNockCAampGroganJ(2011)Theimportanceoftreesizeandfecundityforwinddispersalofbig-leafmahoganyPLoS ONE6e17488httpsdoiorg101371journalpone0017488
PillayRHuaFLoiselleBABernardHampFletcherRJ(2018)DatafromMultiplestagesoftreeseedlingrecruitmentarealteredintrop-ical forestsdegradedbyselective loggingDryad Digital Repositoryhttpsdoiorg105061dryaddk4t694
PoulsenJRClarkCJampBolkerBM(2012)Experimentalmanipula-tionofseedshadowsofanAfrotropicaltreedeterminesdriversofre-cruitmentEcology93500ndash510httpsdoiorg10189010-24301
Putz F E Zuidema P A Synnott T Pena-Claros M Pinard MA Sheil D hellip Zagt R (2012) Sustaining conservation val-ues in selectively logged tropical forests The attained andthe attainable Conservation Letters 5 296ndash303 httpsdoiorg101111j1755-263X201200242x
R Development Core Team (2017) R A language and environment for statistical computing Vienna Austria R Foundation for StatisticalComputing
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352
8242emsp |emsp emspensp PILLAY et AL
RiuttaTMalhiYKhoLKMarthewsTRHuascoWHKhooMhellipEwersRM (2018)Loggingdisturbanceshiftsnetprimarypro-ductivityanditsallocationinBorneantropicalforestsGlobal Change Biology242913ndash2928httpsdoiorg101111gcb14068
SchleuningMFarwigNPetersMKBergsdorfTBleherBBrandlRhellipBoumlhning-GaeseK(2011)Forestfragmentationandselectivelogginghaveinconsistenteffectsonmultipleanimal-mediatedeco-systemprocessesinatropicalforestPLoS One6e27785httpsdoiorg101371journalpone0027785
SoepadmoESawLGampChungRCK (2002)Tree Flora of Sabah and Sarawak Volume 4 (E Soepadmo LG Saw and RCK ChungEds)Kuala LumpurMalaysia SabahForestryDepartment ForestResearchInstituteandSarawakForestryDepartment
Soepadmo EampWongKM (1995)Tree flora of Sabah and Sarawak Volume1(ESoepadmoandKMWongEds)KualaLumpurMalaysiaSabahForestryDepartmentForestResearchInstituteandSarawakForestryDepartment
StollPampNewberyDM (2005)Evidenceof species-specificneigh-borhoodeffects in theDipterocarpaceaeofaBorneanrain forestEcology863048ndash3062httpsdoiorg10189004-1540
StruebigMJTurnerAGilesELasmanaFTollingtonSBernardHampBellD (2013)Quantifying thebiodiversity valueof repeat-edly logged rainforests Gradient and comparative approachesfrom Borneo (eds G Woodward and EJ OrsquoGorman) Advances in Ecological Research 48 183ndash224 httpsdoiorg101016B978-0-12-417199-200003-3
SwamyVampTerborgh JW (2010)Distance-responsivenaturalene-miesstronglyinfluenceseedlingestablishmentpatternsofmultiplespecies in anAmazonian rain forest Journal of Ecology98 1096ndash1107httpsdoiorg101111j1365-2745201001686x
TherneauTM(2015)coxmeMixedeffectsCoxmodelsRpackagever-sion22-5
WearnORRowcliffeJMCarboneCBernardHampEwersRM(2013)Assessingthestatusofwildfelidsinahighly-disturbedcom-mercialforestreserveinBorneoandtheimplicationsforcameratrap
survey designPLoS ONE8 e77598 httpsdoiorg101371jour-nalpone0077598
WebbCOampPeartDR (1999) Seedlingdensitydependencepro-motes coexistence of Bornean rain forest trees Ecology 802006ndash2017 httpsdoiorg1018900012-9658(1999)080[2006SDDPCO]20CO2
WilcoveDSGiamXEdwardsDPFisherBampKohLP (2013)NavjotrsquosnightmarerevisitedLoggingagricultureandbiodiversityinSoutheastAsiaTrends in Ecology and Evolution28531ndash540httpsdoiorg101016jtree201304005
WoodcockPEdwardsDPNewtonRJKhenCVBottrellSHampHamerKC (2013) Impactsof intensive loggingon the trophicorganisationofantcommunitiesinabiodiversityhotspotPLoS ONE8e60756httpsdoiorg101371journalpone0060756
WrightSJ(2002)PlantdiversityintropicalforestsAreviewofmech-anisms of species coexistence Oecologia 130 1ndash14 httpsdoiorg101007s004420100809
ZuurAFIenoENWalkerNJSavelievAAampSmithGM(2009)Mixed effects models and extensions in ecology with RNewYorkNYSpringerhttpsdoiorg101007978-0-387-87458-6
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articlePillayRHuaFLoiselleBABernardHFletcherJrRJMultiplestagesoftreeseedlingrecruitmentarealteredintropicalforestsdegradedbyselectiveloggingEcol Evol 201888231ndash8242 httpsdoiorg101002ece34352