Buildingwooddebrispilesbenefitsavianseeddispersersinburnedand logged
Mediterraneanpineforests
J.Rosta,∗, M.Claveroa,b, J.M.Bas a, P.Ponsa
aDepartamentdeCiènciesAmbientals,UniversitatdeGirona,CampusdeMontilivi,17071Girona,Catalonia,Spain
bGrupd’EcologiadelPaisatge,Àrea deBiodiversitat,CentreTecnològicForestaldeCatalunya,CarreteravelladeSantLlorenc¸ deMorunys,Km2.25280Solsona,Catalonia,Spain
abstract
Keywords: SalvageloggingPostfiremanagement
Winterbirdcommunity
Frugivorousbirds Seeddispersal Pinushalepensis
Salvageloggingisacommonpracticecarriedoutinburned forestsworldwide,andintendedtomitigate theeconomic lossescausedby wildfires.Loggingimpliesanadditionaldisturbanceoccurring shortly afterfire,althoughitsecologicaleffectscanbesomewhat mitigatedbyleavingwooddebrison site.The compositionofthebirdcommunityanditscapacitytoprovideecosystemservicessuchasseeddispersal offleshy-fruitedplantshavebeenshowntobeaffectedbypostfirelogging.Weassessedtheeffectsofthe habitatstructureresultingfromdifferentpostfiremanagementpracticesonthebirdcommunity,inthree burnedpineforestsinCatalonia(westernMediterranean).Forthispurpose,wefocusedon thegroupof speciesthatisresponsibleforseeddispersal,aprocesswhichtakesplaceprimarilyduringthewinterin theMediterraneanbasin.Inaddition,weassessedmicrohabitatselectionbyseeddisperserbirdsinsuch environments in relation tomanagementpractices.Our resultsshowed asignificant,positiverelation- shipbetweenthedensityofwooddebrispilesandtheabundanceofseeddisperserbirds.Furthermore, suchpileswerethepreferredmicrohabitatofthesespecies.This revealsanimportanteffectofforest managementon seed disperserbirds,whichislikelyto affectthedynamicsofbird-dependentseeddis- persal.Thus,buildingwooddebrispiles canbeausefulpracticefortheconservationofboththespecies and theirecosystemservices,whilealsobeingcompatiblewithtimberharvesting.
©2010ElsevierB.V.Allrightsreserved.
1. Introduction
Wildfiresare oneofthemost importantdisturbancesaffecting ecologicalprocessesandeconomicinterestsinforestecosystems worldwide(BlondelandAronson,1999;HessburgandAgee,2003; FAO,2007).Inmanycountriespostfiresalvagelogging(i.e.,thehar-vestingofburnedtimberfor mainlycommercialpurposes)isthe mostextendedforestry practice intendedto compensatefor the economiclossescausedby wildfires(Hutto,2006;Lindenmayer etal.,2004).Salvageloggingisalso justifiedby otherobjectives, suchasreducingthefuel load,enhancingfuturetreesurvival,pre- ventingtheproliferationofxylophagousinsectsormakingiteasier andsaferforpeopletopassthroughtheburnedareaorforfuture forest managementwork to be carriedout(Ne’emanetal.,1995; Martínez-Sánchezetal.,1999;LindenmayerandNoss, 2006).
IntheMediterraneanBasin, wheretherehas beenalonghis- toryoflandscapemanagement,firesoftentakeplacein lowland pineforests,mostofwhichgrowon abandonedagriculturalland (Trabaud,1981).Inthistypeofforest,afterafire, salvagelogging is themostfrequentlyusedmanagementmethod,becausepine
∗ Correspondingauthor.Tel.: +34972418269;fax:+34972418150.
E-mailaddress:(J.Rost).
woodisstill commerciallyprofitablefor use as boardsuntiltwo yearsafterafire, andevenlaterifgrounddown(e.g., to produce biomassfuel). Ingeneralterms,salvagelogginginvolvesadrastic habitatchange—fromaburnedforeststructureto opengrassland andshrubland—ashorttimeafterthefire. However,on asmaller scalethecharacteristicsofthesenewopenhabitatsalsodependon theinterestsanddecisionsoflandownersandmanagers,andthere- foreontheownershipstructureofeachburnedforest.Whenforests are dividedintosmallprivatelyownedlots, asisoftenthecasein Mediterraneanareas,individualdecisionsleadto thecoexistence ofmultiplemanagementmodelsinburnedstandsincloseproxim- ity.Thesestrategiesresultinclearcuts(wherewooddebrismaybe completely removed, left on thegroundorpiled up), areaswhere isolatedsnagsremain,andunloggedstandsof partiallyburned pines.Furthermore,restorationmeasuressuchaslogerosionbar- rierscan be foundin burnedpublicforests,whichare managed essentiallyfor restorationpurposes.The administrativeauthor- ityconcernedmayalso issuemanagementrecommendations,and grantsubsidiesto,orreachagreementswith,locallandowners,who maythendelegatepostfiremanagement topublicmanagers.
The habitatdisturbanceinduced bypostfiresalvagelogging affectsanimalcommunities,anissuethathassometimesbeenstud- ied usingbirdsas thefocal group(Kotliaretal.,2002;Huttoand Gallo,2006;CahallandHayes,2009).Ithasbeenshownthatsalvage
Fig. 1. Locationof thethreestudyareasanddistributionof the76stations(dots)withintheseareas(CI: Cistella;TM: TorroelladeMontgrí;VE: Ventalló).Grayareas correspondtotheformerforestszonesonwhichthestudyfocused.FireperimetersobtainedfromDMAH (2008).
logging can haveagreaterimpactthanthefire itselfontheforest birdcommunity,includingthesubstitutionofforestspecialistsby open-landspecies(Izhaki,1993;Llimonaetal.,1993;Morisetteet al.,2002;Castroetal.,inpress).Such changesare likelyto affect frugivorousbirdspecies,someofwhichare involvedinimportant ecologicalprocessessuchasseeddispersaloffleshy-fruitedshrubs andclimbers.IntheMediterranean,fleshy-fruitedplantsproduce ripefruitduringthefallandwinter(MooneyandKummerow,1981; Jordano,1992),whenvariousspeciesofsmallandmedium-sized birdsdispersetheirseeds(Herrera,1984,1998).Inburnedareas, earlysuccessiongivesrise to a shrubland-likehabitat(Trabaud andLepart,1980),whichhostsadiversewinterbirdassemblage, includingsomespeciesthatattainhighdensitiesthanksto post- fire fruitandseedproduction(PonsandProdon,1996;Pons,2001; Telleríaetal.,2004).IzhakiandAdar (1997)showedthatwinter bird communities ineasternMediterranean burnedandlogged forestsweredominatedbyshrublandspecies,someofwhichwere seeddispersers.However,thehabitatandmicrohabitatuseofthese speciesunderdifferentscenariosofpostfire managementhas not yetbeenstudiedindepth.Previousstudieshavereportedthatbird- dependentseedrainstronglyreliesonhabitatstructuresthatactas dispersalfoci,suchasisolatedtreesthatactasperches(Guevaraand Laborde,1993;Pausasetal.,2006;HerreraandGarcía,2009). After logging,wooddebrispiles andbarriersbuiltinaburnedpineforest canalso actasdispersalfoci(Rost etal.,2009).Thus, thevariability ofpostfiretreatmentsafterlogging,whichleadstothepresenceof differentmicrohabitatsonasmallscale,mayhaveimportantimpli- cationsforbird-dependentseedrain,dependingonthedifferential use thatseeddispersersmakeoftheresultingmicrohabitats.
Theaimsofthisstudyare:(1)toinvestigatetheeffectsofpostfire managementonwinterbirdcommunitiesinburnedMediterranean pineforests,(2)todeterminewhethercertainmanagementprac- ticeshavepositiveeffectson speciesrichnessandabundanceof seeddispersersin winter,and(3) to analyzemicrohabitatselec- tionbyseeddispersersinordertodescribepatternsintheiruse of themicrohabitats.Ifpostfiremanagementpracticeshadan effect on seeddispersersdistributionandmicrohabitatuse, thiswould also affectseedrainandtheregenerationoffleshy-fruitproduc- ingshruborclimberspecies.Wetookadvantageofthe availability
inthreestudyareasofexamplesofdifferentpostfireloggingprac- tices(rangingfromcompletelyloggedareastounloggedones,and includingdifferentmethodsofmanagingwooddebris)toinvesti- gatewhichof thesepracticesmaybemorefavorabletothepresence ofbirdspeciesinvolvedinseeddispersal.
2. Methods
2.1. Study area
The studywascarriedoutin threeburnedareaslocatedin Catalonia,in thenortheastoftheIberianPeninsula:Torroellade Montgrí(henceforthTM,3◦7tE,42◦3tN),Ventalló(VE,3◦2tE,42◦7t N) andCistella(CI,2◦50tE,42◦17tN) (Fig.1).Themaximumdistance betweenany twoareaswas30km. Allthreeareashaveameso- Mediterraneanclimate,limestone substrates,andaltitudesranging from80 to 210m abovesea level.Beforethefire, theyfeatured avegetationmosaiccomposedofAleppopine(Pinus halepensis) forests,shrublandandcrops.TMburnedin September2004and thefire affected188ha ofpineforest;in VEandCIfiresburned
613 and170ha of pineforest,respectively,in August 2006. All wereseverefiresthataffectedforestcanopyandundergrowth, andasaresultthevastmajorityofpinesdiedandtheshrubcover disappeared.
PropertiesatVEandCIstudyareasare smallandprivately owned. InVE96%oftheareaisinprivateownership,withstands ranging inareafrom0.5to5ha andonlyafew standslargerthan
15ha,whileinCI100%oftheareaisinprivateownership,withone standof80ha andtherestrangingfrom5to20ha. Inbothareas salvageloggingstartedduringthefirstwinterafterthefires and wasstill happeningwhenthefieldworkwasconducted,affecting approximately 60%oftheburnedforestareainVEandabout75% inCI.The few forestpatcheswherepinessurvivedafterthefires wereleftunlogged.Inafew areas,non-profitablewooddebriswas heapedup insmall,low piles.InTM,thepredominanceofpublic ownership(66%ofthetotalarea)led to patchypostfiremanage- ment,includingbothloggedandunloggedareasandrestoration measures.Inloggedpatches,however,afew standingsnagswere preserved(ca.10snags/ha)andlogbarrierswerebuiltup against
Fig. 2. Templateusedtoestimatethescatteredwooddebriscoverontheground.
runoffanderosionbypilingtrunksandbranchesalongthecontour lines(thesizesofthepilesbeing0.5–1m highand3–10m long) (Rost etal.,2009).Bythetimewe conductedthefieldworkinTM allunloggedsnagshadfallendown,ashadalmostathirdofthose inVEandCI.
Thestudywasconductedinwinter2008–2009,thethirdwinter afterthefires in VEandCIandthefifth in thecaseofTM,when vegetationwasinearlysuccession.Theregeneratingundergrowth wascomposedofresprouterandseedershrubs(Quercuscoccifera, Phillyreaangustifolia,Cistus spp.)andherbs(Brachypodiumspp.), withyoungAleppopinesaplings inmanystands.Weconcentrated allfieldworkinasinglemonth(January)inordertoavoidasmuch aspossiblethechangesinbirdabundancethatmayhappenalong winter.
2.2. Birdsampling
Wedistributed74samplingstationsof100mradiusinthestudy areas,followingaregularspatialdistributionwithintheburned forests(48stationsinVE,17inTMand9inCI;Fig.1).Whenchoos- ing theexactlocationof thestationswe borein mindto allow aminimumdistancebetweenstationcenters(300m), toensure goodvisibility,andtosampleahomogeneoushabitat(burnedfor- estwiththesamemanagementmodel).Recentlyloggedareas(less thanfour weeksafterlogging)werenotsampledinordertoavoid thedisturbancethatloggingwork mighthavecausedtothebirds. Birds werecountedusingthepointcountmethod(Bibby etal.,
1992)onceateachstation.Allcountswereperformedbythesame observer,conductedbetween1and4hafterdawnandundergood weatherconditions.Allbirdsseenorheardwithina100mradius duringthreeconsecutive5-min periodswereregistered,butindi- vidualsseenjustflyingoverwerenotcounted,as theywerenot consideredtobeusingthesampledhabitat.Inordertoreducethe probabilityofdoublecountsduringthe15min,wecomputedeach species’abundanceasthemaximumnumberofindividualsinany ofthethree5-minperiods.Weinitiallyseparatedbirdobservations inthreedistancebandsfromtheobserver(0–25m, 25–50m and
50–100m) to accountfor detectability.However,theestimation
ofdetectionprobabilitieswithDistance5program(Thomasetal.,
2006)wasonlypossibleforthe42%mostfrequentspecies.Forthese species,birddensitytakingintoaccountdetectionprobabilitywas highlycorrelatedwith therawabundance(R2=0.83).Moreover,at least67% ofdetectionsofthespeciesthataccountedfor75% ofthe totalabundancewhere auditory,sothat birdsweredetectedrather irrespectivelyofthecoverstructure.Forthesereasonsweusedraw abundancesinalltheanalyses.
2.3. Habitatvariables
Habitatvariablesrelatedto vegetationrecoveryandpostfire managementwererecordedateachstation.Withina20mradius areacenteredon thestationwe estimatedtherelativearea(in percentage)coveredby:bareground,vegetationupto0.25m,veg- etationup to 0.5m, vegetationup to 1m, andvegetationhigher than1 m (excludinglive trees),whichall togethertotalled100%. Thedensityandcoverofstanding snagsandlive treesweremea- suredin a 20m radiusarea(if densitywas>100trees/ha),50m radiusarea(between10 and100trees/ha)or 100m radiusarea (<10trees/ha).Thedensity(number/ha)andcoverofwooddebris pilesorbarriersina50mradiusarea,andthecoverof loggingdebris scattered on thegroundina20mradiusareawereconsideredas managementvariables.Cover measureswereestimatedbyvisual comparisonwiththetemplateusedbyProdonandLebreton(1981), exceptforscatteredwooddebris,forwhichwe designedaspecific template(Fig.2).
2.4. Microhabitatselectionbyavianseeddispersers
Asa resultof thepostfiremanagementexplainedabove,we definedfive different microhabitatcategories: live trees, standing snags,regeneratedshrubs,wooddebrispiles,andbareground.The availabilityofeachmicrohabitatwasestimatedasitscover(inper- centage)withinthestation.Duringpointcounts,we recordedthe microhabitat (onlyoneineachcase)inwhichindividualbirdswere detected.Forflushedoutindividuals,we recordedthemicrohabi- tatfromwhichtheyhadflownaway.Whenthiswasnotpossible
(e.g.,inthecaseofwood pilesamongliveshrubsandbareground patches),thesecondsitewherethebirdstoppedwasrecorded, sincethefirst movementmighthavebeeninfluencedbythepres- enceof theobserver. The behaviorof seeddisperser speciesof fleshy-fruitedplantswasalso recorded,categorizedas foraging, perching,shelteringorunknown(whenabirdhadbeenflushedout andnotrelocated).Onlythosespeciesclassifiedasmajordispersers inHerrera(1995),thatis,allspeciesofthegenusSylviaandTurdus plustheEuropeanrobin(Erithacusrubecula),wereconsideredas seeddispersersintheanalyses.
2.5. Data analyses
Multivariateanalyseswereusedto exploretherelationships betweenbirdcommunityandhabitatstructure.Allspeciesoccur- ringin<5%ofpointcountswereexcluded.A redundancyanalysis (RDA) wasappliedto thespeciesandto thehabitatandman- agementvariablesmatrices,includingburnedareaasacovariate. Aforwardselectionofhabitatvariables wasperformedusing Monte–Carlopermutationtestsandincludingthosevariablesthat weresignificantatap0.1 level.IntheRDA,twospeciesoccur- ringin3–5%ofthe pointswereincludedassupplementaryspecies (thusnotinfluencingtheanalysisresults).TheseweretheEuro- peanjay (Garrulusglandarius),because of its importanceas oak acornsdisperser,andtheSoutherngreyshrike(Lanius meridion- alis),becauseoftheinterestinitsconservationinEurope(BirdLife International,2004).We usedalinearmethod(RDA)insteadofa unimodalapproachbecausethelengthofthegradientofaDCA performedto the20 speciesand74 samplesmatrixwas2.75 SD, suggestingamostlylinearresponseofthespecies(terBraakand Smilauer,1998).RDAandDCAwereperformedwith CANOCO(ter BraakandSmilauer,1998).APrincipalComponentsAnalysis(PCA) withvarimaxrotationwasperformedtoresumehabitat variability inareducednumberofhabitatgradients.Thevariablesusedwere bare ground,allthelivevegetationcategoriesdefinedabove,snag density,andlivetreedensity.Weinterpretedthemeaningofprin- cipalcomponentsusingvariableswithfactorloadingshigherthan
0.6,inabsolutevalue.PCAgradientswerekepttobeusedaspredic- tor variablesinsubsequentanalyses.WeusedStatistica6(Statsoft Inc.,2001)toperformthis analysis.
Generalizedlinearmixedmodels(GLMM)wereusedto assess theimportanceofhabitat-managementvariablesonthefollowing communityvariables:abundanceandspeciesrichnessoftheover- all birdcommunity,andabundanceandspeciesrichnessofseed dispersers.Abundancesofmostcommonseeddisperserswerealso analyzed. We usedfirsttwo PCAgradients,scatteredwooddebris coverandpilesdensityaspredictors.GLMMwithPoissonerrorand linklogwereperformed,includingthelocalityasarandomfactorin ordertocontrolpossiblesite-baseddifferences.Foreachdependent variable,theminimumadequatemodelwasselectedfollowinga manualbackwardselectionprocedure,retainingthosepredictors withp-valuessmallerthan0.05.GLMMswereperformedwithpro- gramR2.9.2 (RDevelopmentCore Team,2009), usingthelme4 software.
Microhabitatselectionbyseeddisperserbirdswasanalyzedfor theoverallseeddispersersgroupand forthethreemostabundant seeddisperserspecies(Sardinianwarbler[Sylvia melanocephala], Dartfordwarbler[Sylviaundata]andEuropeanrobin)bycompar- ing observedandexpectedbirdobservationfrequencies in each microhabitatwithchi-squaretests.Expectedfrequencieswerecal- culatedfromtheavailabilityofmicrohabitatsinthestationswhere thespecieshadbeendetected,afterscalingthesemicrohabitats’ coverto 1.Behaviorwasnotincludedin theanalysesdueto the excessivereductionoffrequenciesthatwouldbeinvolvedbydoing so,and wasonlyrepresentedgraphically.
3. Results
In thepointcountswe recordedatotalof744 birdsbelong- ing to 38 species(Table1). The mostabundantspecieswerethe Sardinianwarbler,theDartfordwarbler,theEuropeanrobin,the Hedgeaccentor(Prunellamodularis)andtheChaffinch (Fringilla coelebs).The seeddispersergroupis composedby ninespecies (Table1),whichaccountedfor58%ofthetotalabundance,thethree mostabundantaccountingfor48%ofthe totalabundance.
RDAresultsshowedthathabitatvariablesexplained16%of thetotalvarianceof thespeciesdataset,andthefirsttwoaxes explained87%ofthespecies-environmentrelationships(eigenval- ues:firstaxis=0.08, secondaxis=0.04).Covariatesexplainedan additional9%ofthevariance.Theordinationofspeciesalongthese twoaxesshowstwomaingradients, onerelatedto regenerated vegetationstructureandtheotherrelatedto thedensityofsnags andlive trees(i.e., theloggingintensity)(Fig.3). The firstgradi- entseparatesspeciesthatrequireopenareaswith low vegetation cover,suchastheWoodlark(Lullulaarborea),fromthosethatdwell inwell-developed,highshrubland,suchastheSardinianwarbler andtheBlackcap.Thesecondaxisseparatesforestspeciesthatpre- ferhightreedensity,suchasParustitsorChaffinches,fromthose thatmainlyselectunwoodedhabitatsinwinter,whichisthecase oftheDartfordwarbler,theEuropeanrobinortheZittingcisticola (Cisticola juncidis).
Thefirstaxis ofthePCAexplained29%oftotalvarianceinhabi- tatcharacteristics(eigenvalue=2.04),andwaspositivelyrelatedto vegetationup to 1m andhigherthan1m, andnegativelyto bare groundandvegetationup to 0.25m. The secondaxis explaineda further21%ofthevariance(eigenvalue=1.50),andwaspositively relatedto snagdensityandvegetationup to 0.5m. The firstfac- tor thusrepresentedundergrowthstructuresrangingfromopen areasto highshrublands,whilethesecondorderedsamplesfrom clearcutstoareaswithhighsnagdensity.
Fig.3. BiplotofthefirsttwoaxesoftheRDA,showingspeciesandsignificantenvi- ronmentalvariables(livevegetationupto0.25m, livevegetationhigherthan1m, snag densityandlivetreedensity).Trianglemarksindicateseeddisperserspecies. Speciesabbreviations areshowninTable1.Theinsetgraph(topleft)showsthe ordinationofsamplesalongthesameaxes,withdotsrepresentingthestudyareas (black-TM;gray-CIandwhite-VE).
Table1
Speciesrecordedinall 74pointcountswithoccurrenceandtotalnumberofindividuals.Asterisksshowseeddisperserspecies(Herrera,1984)offleshy-fruitplants,and doubleasterisksshowmajordisperserspecies(Herrera,1995).Thehorizontalbarseparatesthosespeciesconsideredinmultivariateanalysesfromthosenotconsidered.
EnglishnameScientificnameAcronymOccurrenceSumofcounts
Sardinianwarbler** / Sylviamelanocephala / SYME / 71 / 191Dartfordwarbler** / Sylviaundata / SYUN / 52 / 93
Europeanrobin** / Erithacusrubecula / ERRU / 48 / 74
Hedgeaccentor / Prunellamodularis / PRMO / 33 / 44
Winterwren / Troglodytestroglodytes / TRTR / 26 / 29
Chaffinch / Fringillacoelebs / FRCO / 24 / 43
Greattit / Parusmajor / PAMA / 20 / 30
Chiffchaff / Phylloscopuscollybita / PHCO / 16 / 16
Woodlark / Lullulaarborea / LUAR / 15 / 24
Songthrush** / Turdusphilomelos / TUPH / 13 / 28
Blackcap** / Sylviaatricapilla / SYAT / 12 / 19
Bluetit / Paruscaeruleus / PACA / 12 / 17
Blackbird** / Turdusmerula / TUME / 11 / 14
Zittingcisticola / Cisticolajuncidis / CIJU / 10 / 12
Crestedtit / Paruscristatus / PACR / 8 / 10
Short-toedtreecreeper / Certhiabrachydactyla / CEBR / 8 / 11
GreatSpottedwoodpecker / Dendrocoposmajor / DEMA / 6 / 6
Stonechat* / Saxicolatorquatus / SATO / 6 / 7
Commonkestrel / Falco tinnunculus / FATI / 4 / 4
Woodpigeon / Columbapalumbus / COPA / 4 / 12
Europeanjay* / Garrulusglandarius / GAGL / 3 / 4
Commonbuzzard / Buteobuteo / BUBU / 2 / 2
Meadowpipit / Anthuspratensis / ANPR / 2 / 2
Long-tailedtit / Aegithaloscaudatus / AECA / 2 / 5
Southerngreyshrike / Laniusmeridionalis / LAME / 2 / 2
Goldfinch / Cardueliscarduelis / CACD / 2 / 6
Serin / Serinusserinus / SESE / 2 / 11
Cirlbunting / Emberizacirlus / EMCI / 2 / 2
Peregrinefalcon / Falco peregrinus / FAPE / 1 / 1
Hoopoe / Upupa epops / UPEP / 1 / 1
Greenwoodpecker / Picusviridis / PIVI / 1 / 1
Alpineaccentor / Prunellacollaris / PRCO / 1 / 3
Bluerock-thrush / Monticolasolitarius / MOSO / 1 / 1
Mistlethrush** / Turdusviscivorus / TUVI / 1 / 1
Greenfinch / Carduelischloris / CACH / 1 / 2
Linnet / Cardueliscannabina / CACN / 1 / 1
Redcrossbill / Loxiacurvirostra / LOCU / 1 / 2
Cornbunting / Miliariacalandra / MICA / 1 / 13
Fig. 4. Effectofpiledensityonoverallcommunityandseeddispersersabundanceandspeciesrichness.Onlymajorseeddispersershavebeenconsidered(Herrera,1995). Thedashedlinerepresentsthelinearregressionline.
Table2
SummaryofGLMM selectedmodelsanalyzingtheeffectofhabitatandmanagementvariables(PCA1, PCA2, piledensityandscatteredwood debriscover)ontheoverall communityabundanceandrichness,majordisperserabundanceandrichnessandmostcommonmajordisperserspeciesabundance,usinglocalityasarandomfactor. Explainedvarianceisshownasthevariationindeviancebetweennullandselectedmodels,whenbothdiffered.
Responsevariable / Explainedvariance(%) / Predictors / Estimate / pOverallcommunity
Abundance / 4.3 / PCA2 / −0.090 / 0.016
Richness / 0.0 / – / – / –
Majorseeddispersers
Abundance / 5.3 / Pile density / 0.009 / 0.017
PCA1 / 0.141 / 0.005
PCA2 / −0.116 / 0.030
Richness / 9.6 / Pile density / 0.009 / 0.088
Sardinianwarbler / 10.8 / PCA1 / 0.200 / 0.006
Dartfordwarbler / 4.7 / Pile density / 0.016 / 0.026
Europeanrobin / 6.2 / Pile density / 0.023 / 0.003
Blackcap / 15.0 / Pile density / 0.042 / 0.003
Blackbird / 0.0 / – / – / –
Songthrush / 0.0 / – / – / –
Theoverallbirdabundancewashigherinareasoflow density ofsnagsandlive trees,whileoverallrichnesswasnotaffectedby any habitat-managementpredictor.The abundanceof seeddis- perserswaspositivelyrelatedto pile density(Fig. 4) andshrub coverandnegativelyto snagdensity,andtheirspeciesrichness wasnotaffectedbyany predictor.Shrubcoverwasalso relatedto theabundanceoftheSardinianwarbler, themostcommonseed disperser.Inadditiontoinfluencefrugivoresabundance,pile den- sity favoredtheoccurrenceoftheDartfordwarbler,theEuropean robin,andtheBlackcap(Sylviaatricapilla).Ontheotherhand,Tur- dus thrushesdid notshowany habitat-managementpreferences. SeeTable 2forfurtherdetailsandsignificancevalues.
Both the seeddispersergroupand the three most abun- dantspecies(Sardinianwarbler,DartfordwarblerandEuropean robin)usedavailablehabitatelementsin anon-randomfashion (Fig.5). Asagroup, seeddispersersweremostfrequentlyfound on piles,resproutingshrublandandsnags,usingpilesandsnags morethanwouldbe expectedfromhabitatelementavailability
(x2 =643.16,p0.01).Intermsofindividualspecies,theSardinian
Warbler,DartfordWarblerandEuropeanRobinpreferedwoodpiles morethanexpected(x2=258.14,p0.01;x2=100.03,p0.01,and x2=173.10,p0.01, respectively).Behaviorobservationsrevealed thatbirdspeciesusedtheseelementsforsomewhatdifferentpur- poses,withSardinianandDartfordwarblersusingpilesandshrubs basicallyforforaging,andEuropean robinsmostlyforperching.
4. Discussion
Habitat heterogeneityinburnedMediterraneanpineforests allowsthecoexistenceof birdspecies withdifferenthabitat requirementsduringwinter,andthuswefoundamixtureofopen- land,shrublandandforestbirdsin our studysites.Such habitat andbirdcommunityheterogeneitylikelyresultsfromthemanage- mentcarriedoutintheseareas,aswellasfromtheregeneration of thelow plant cover.We foundthat differentmanagement practicesfavoreddifferentbirdspeciesin winter.Indeed,man- agersdecisions,suchastheextentofsnagloggingandhowwood debrisis managed,thatdependbothon theirobjectives(har- vest/restoration)andon thesmallsize oflots inthearea,greatly affectwhichbirdspecieswill occupythearea.Thus, strictopen- landbirdsmaytakeprofitbothfromfire, whichcreatesopenareas oflow herbsandbareground,andfromlogging,becauseofthe mechanicaldamagetoligneousvegetation associatedwithlogging operations,whichhindersproperregeneration(Martínez-Sánchez etal.,1999;Van Nieuwstadtetal.,2001;LindenmayerandNoss,
2006).Shrublandbirdsdwellintheregeneratedshrubsandbushes
thathavegrownsincefireandloggingoccurred,aswellasinnewly builtwoodpilesandbarriers.Intheseclearcutscreatedbysalvage logging,winterbirdabundanceishigherthaninunloggedpatches wheresnagshavebeenretained.However,unloggedareasallow thepersistenceofsomeforestspeciesthatdonotoccurwhen snags are logged.
Almosta quarterof all birdspeciesandmorethanhalf of theindividualsdetectedin thestudyareawereseeddispersers, andamongthem,theSardinianandDartfordwarblersandthe Europeanrobinwerethemostfrequentspecies.Ingeneral,Sylvia warblersoccurredmainlyin bushyhabitatswithoutsnagsand trees.However,theyshowedsomedifferencesin habitatprefer- encesinaccordancewiththeirrequirements(Shirihaietal.,2001), becauseDartfordwarblerswerefoundin lower shrublandthan SardinianwarblersandBlackcaps.TheEuropeanrobinwasfound insimilarhabitatsto thoseofwarblers,sincewinteringindividu- als can occurinmoreopenanddrierhabitatsthanbreedingones (Cramp,1998).Ontheotherhand,Turdusthrusheswerenotclosely linkedto any specifichabitat,buttheSong thrushseemedmore relatedtothepresenceofsnagsandlivetrees.Bycontrast,Castroet al.(inpress)foundthatinMediterraneanmontanepineforests,Tur- dus thrusheswerethemostabundantseed disperser/frugivorous speciesinwinter,theEuropeanrobinwasabsent,andSylviawar- blerswereuncommon.Salvageloggingcan thushavedifferent effectson theseeddispersersgroupdependingon thealtitude, probablybeing moredetrimentalfor seeddispersersin montane thaninlowlandforests.
Themostremarkableresultofour studyisthatseeddispersers are moreabundantwherepilesof burnedwoodare builtup in largequantities,beingparticularlyimportantforDartfordwarblers, EuropeanrobinsandBlackcaps.Theverticalstructureofthesepiles orbarriersmaygivethemtheappearanceofshrubpatchesandthus attractbirdsin earlysuccessional vegetationstages(Herrandoet al.,2009),andseemedalso to be important structures forspecies suchas theEuropeanrobinthatare usedto perchingfrequently whenforaging,or as partof theirterritorialbehavior.Further- more,theoccurrenceofmacro-arthropodsincoarsewood debris (Grove,2002;Jabin etal.,2004;Varady-SzaboandBuddle,2006) mayincreasetheuse ofpilesbyinsectivorousspecies.Inaddition, thepreferenceforpilesshownbyfrugivorousbirdsmayhaveinter- estingecologicalimplicationsfor theseedrainprocessinburned andmanagedareas,andsupporttheroleplayedbypilesasseeddis- persalfoci(Rost etal.,2009).If dispersedseedscan germinateand surviveunderpiles,apositiverelationshipbetweentheabundance offleshy-fruitedplantsandoffrugivorousbirdsislikely,sincepiles maylaterhostagreaterabundanceofsuchplants,andthusbecome importantfeedingpointsforfrugivorousbirds.However,thepos-
Fig. 5. Relativefrequenciesofmicrohabitatuseby all majordisperserspecies,theSardinianwarbler(SYME), theEuropeanrobin(ERRU) andtheDartfordwarbler(SYUN). Foreachhabitatelement(GR,ground;PI,pile;SH,shrub;SN,snag;LT,livingtree),theleftbarshowsobservedfrequenciesfor fourbehaviorcategories,whiletherightwhite barshowsexpected frequencies(foreverygraph,observedandexpected frequenciesaddup 100%).Thenumbersabovethebarsshowthenumberofobservedorexpected frequenciesfor each category.
siblelink betweenpilesandfruitavailabilityisasubjectstill to bestudied.Apartfromthis,anotherwaytodealwithwooddebris isto leaveit scatteredon theground.Our resultsshowthatthis management methoddid nothaveabigeffecton thefrugivorous guild.
Buildingwooddebrispilesin burnedandloggedareasmay thereforebean importantfactorforfleshy-fruitedplants, ifafter- wardsthesestructuresbecomepointsofhighdensitiesofdispersed andestablishedplants.Thiscouldleadtoaheterogeneousdistribu- tion ofdispersedplantspecieswithinburnedloggedareaswhere pileshavebeenbuiltup.Seed disperserbirdscan bringseedsfrom unburnedneighboringareas,wheretheymayhaveeatenfruit,into burnedareas(Rost etal.,2009).The arrivalofmigrantfrugivores andthelossofterritorialbehavioroflocalonesduringwintercould allowlongerdispersaldistancesthan inspring-summer,whenseed dispersalbybirdstakesplaceonlyatshortdistances(i.e.,mostly below100m) (Jordanoetal.,2006).Therefore,birdsattractedto burnedareasbythepresenceofwooddebrispilescouldfacilitate thecolonizationoftheseareasbythedispersedplantspecies,with possiblepositiveconsequencesfor therecoveryofthevegetation afterfire.
Theimplications,suggestedhere,oftheeffectofmanagement practicesonseeddisperserbirdsandontheseeddispersalprocess, are also likelytoapplytoforestsalteredbyotherharvestingprac- tices.CommonforestmanagementmeasuresintheMediterranean, suchasundergrowthclearingandtreethinning,intendedto pro- duceopenforeststandsforpasture,tomaximizetimberproduction ortoreducetheriskoffirebyeliminatingthefuelload,arelikelyto causesuchchanges.Someexistingstudiesofthesemanagement techniquesandbirdcommunitiesin theMediterraneanregion (CamprodonandBrotons,2006;DeLaMontan˜aetal.,2006)found thatsomemajorseeddispersers(Sardinianwarbler,Blackcap,Gar- denwarblerSylviaborin andBlackbird)disappearordecline locally whenshrubclearingand thinningoccur.Thismaymeanadisrup- tionintheseeddispersalprocessinsuchmanagedareasbecause ofthelack ofdispersers,negativelyaffectingbird-dispersedplant
species.Insuchsituations,pilingupcut branchesandotherwoody debriscouldthereforebeseenaspalliativemeasures,becausethey may provideshrubland-dwellingseeddisperserbirdswithsome resourcesthatmayfavortheirsitetenacity.
4.1. Managementrecommendations
Our resultssuggestthat theabundanceanddistributionof birdspeciesinburnedlowland pineforestsinthewestern Mediterraneanduringthewinteris stronglyinfluencedby the implementationofpostfire forestmanagementpractices.Asshown in our results,ifmanagersandlandownersdecideto harvestthe burnedpines,thefate ofwooddebris(branchesandnon-profitable logs) isnotatrivialissueforbirds,becauseitaffectstheabundance ofmajorseeddisperserspecies.Our recommendation,sincescat- teredwood debrishas no effecton birdsabundance,isto collect andheapitupinpilesofatleast0.5mhigh.Around15–25piles/ha couldbe an appropriatedensityto allowthepersistenceofseed disperserbirdsinwinter.Furthermore,woodpiles,iffoundinan appropriatedensity,also haveapositiveeffectonthe speciesrich- nessandabundanceofbreedingbirdspecies(Herrandoetal.,2009), on theabundanceofsomespeciesofrodents(HaimandIzhaki,
1994;ManningandEdge, 2008),andeven ontheEuropeanrabbit (Catalánetal.,2008;JoanReal,pers.comm.),akeystoneofMediter- raneanecosystems.Inmostcases,themainpurposeofbuildingup wooddebrispilesistoreducesoillossbyerosion(Robichaudetal.,
2000),althoughitisnotclearthattheyare usefulforthatpurpose (RaftoyannisandSpanos,2005;MarquesandMora,1998).Never- theless,theirvaluefor birdsandotherfaunawouldjustifytheir inclusioninpostfiremanagementplansaimingtorestorethehabi- tatorintroduceenvironmentallyfriendlymeasures.Suchpractices seemfeasibleinpublicpineforestswherepostfiremanagementis notsocloselylinkedtoeconomicimperatives,andcouldbemade arequirementto obtainpublicsubsidiesfor themanagementof privateforests. Includingthebuildingup ofwooddebrispilesin postfiremanagementguidelinescouldthusbecomean important
factorinhelpingto conservebothspeciesandanimal-dependent ecologicalservicesin theMediterranean region.Finally,dialogue withlandownersofburnedforestsisanecessarysteptofindways tomakeeconomicobjectivescompatiblewiththebenefitsofbio- diversity,thusfacilitatingthemaintenanceofimportantecological functionssuchasbird-dependentseeddispersalprocesses.
Acknowledgements
The authorswouldlike to thankDavidMeyaandJoan Real for kindlyprovidingus withadviceandinformation.This study wasfundedby theSpanishMinistryof ScienceandInnovation (CGL2005-0031/BOSandCGL2008-05506/BOS)andJ.R.heldaFPU grantoftheMinistryofEducation.
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