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Abstract

Aim Natural disturbances influence forest structure, successional dynamics, and, consequently, the distribution of species through time and space. We quantified the long-term impacts of natural disturbances on lichen species richness and composition in primary mountain forests, with a particular focus on the occurrence of endangered species. Location Ten primary mountain spruce forest stands across five mountain chains of the Western Carpathians, a European hotspot of biodiversity. Methods Living trees, snags, and downed logs were surveyed for epiphytic and epixylic lichens in 57 plots. Using reconstructed disturbance history, we tested how lichen species richness and composition was affected by the current forest structure and disturbance regimes in the past 250 years. We also examined differences in community composition among discrete microhabitats. Results Dead standing trees as biological legacies of natural disturbances promoted lichen species richness and occurrence of threatened species at the plot scale, suggesting improved growing conditions for rare and common lichens during the early stages of recovery post-disturbance. However, high-severity disturbances compromised plot scale species richness. Both species richness and the number of old-growth specialists increased with time since disturbance (i.e. long-term uninterrupted succession). No lichen species was strictly dependent on live trees as a habitat, but numerous species showed specificity to logs, standing objects, or admixture of tree species. Main conclusions Lichen species richness was lower in regenerating, young, and uniform plots compared to overmature and recently disturbed areas. Natural forest dynamics and its legacies are critical to the diversity and species composition of lichens. Spatiotemporal consequences of natural dynamics require a sufficient area of protected forests for provisioning continual habitat variability at the landscape scale. Ongoing climatic changes may further accentuate this necessity. Hence, we highlighted the need to protect the last remaining primary forests to ensure the survival of regionally unique species pools of lichens.
J Veg Sci. 2021;32:e13087.    
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https://doi.org/10.1111/jvs.13087
Journal of Vegetation Science
wileyonlinelibrary.com/journal/jvs
Received:8March2021 
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Revised:23July2021 
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Accepted:22September2021
DOI : 10.1111/j vs.130 87
RESEARCH ARTICLE
The impact of natural disturbance dynamics on lichen diversity
and composition in primary mountain spruce forests
Thomas Langbehn1| Jeňýk Hofmeister1| Marek Svitok1,2 | Martin Mikoláš1,3 |
Radim Matula1| Josef Halda4| Kristýna Svobodo1| Václav Pouska1|
Ondrej Kameniar1| Daniel Kozák1| Pavel Janda1| Vojtěch Čada1|
Radek Bače1| Michal Frankovič1| Ondřej Vostarek1| Rhiannon Gloor1|
Miroslav Svoboda1
©2021InternationalAssociationforVegetationScience
1DepartmentofForestEcology,Czech
UniversityofLifeSciencesPrague,Prague,
CzechRepublic
2DepartmentofBiolog yandGeneral
Ecology,TechnicalUniversit yinZvolen,
Zvolen,Slovakia
3PRALES,Rosina,Slovakia
4DepartmentofBiolog y,Universityof
HradecKrálové,HradecKrálové,Czech
Republic
Correspondence
JeňýkHofmeister,DepartmentofForest
Ecology,FacultyofForestr yandWood
Sciences,CzechUniversityofLife
SciencesPrague,Kamýcká129,Praha6
–Suchdol16521,CzechRepublic.
Email:jenyk.hofmeister@email.cz
Funding information
Thisprojectwassuppor tedbytheCzech
ScienceFoundation(GrantGACRno.
31-27454S)andinstitutionalproject
MSMT(CZ.02.1.01/0.0/0.0/16_019/0
000803)andtheCzechUniversityof
LifeSciences(IGAA1917andCIGANo.
20154316).MSvitokwassupportedby
theOperationalProgrammeIntegrated
Infrastructure(OPII),fundedbytheERDF
(ITMS313011T721).
Co-ordinating Editor:MonikaWulf
Abstract
Aim: Naturaldisturbancesinfluenceforeststructure,successionaldynamicsandcon-
sequently,thedistributionofspeciesthroughtimeandspace.Wequantifiedthelong-
termimpacts of naturaldisturbances on lichenspeciesrichnessand composition in
primarymountainforests,with aparticular focusonthe occurrence of endangered
species.
Location: Tenprimarymountainspruceforeststandsacrossfivemountainchainsof
theWesternCarpathians,aEuropeanhotspotofbiodiversity.
Methods: Livingtrees,snagsanddownedlogsweresurveyedforepiphyticandepix-
yliclichensin57plots.Usingreconstructeddisturbancehistory,wetestedhowlichen
species richness and composition wasaffected by thecurrentforeststructure and
disturbanceregimesinthepast250years.Wealsoexamineddifferencesincommu-
nity composition among discrete microhabitats.
Results: Deadstandingtreesasbiologicallegaciesofnaturaldisturbancespromoted
lichen species richness and theoccurrence of threatenedspeciesat theplot scale,
suggesting improved growing conditions for rare and common lichens during the
earlystagesofrecoverypostdisturbance.However,high-severitydisturbancescom-
promised plot-scale species richness. Bothspeciesrichness andthe numberofold-
growthspecialistsincreasedwithtimesincedisturbance(i.e.,long-termuninterrupted
succession).Nolichenspecies was strictlydependentonlivetreesasahabitat,but
numerousspeciesshowedspecificitytologs,standingobjectsoranadmixtureoftree
species.
Conclusions: Lichenspecies richnesswaslowerinregenerating, younganduniform
plotscomparedwithovermatureandrecentlydisturbedareas.Naturalforestdynamics
anditslegaciesarecriticaltothediversityandspeciescompositionoflichens.Spatio-
temporal co nsequences of natura l dynamics require a su fficient area of prote cted
forestsforprovisioningcontinualhabitatvariabilityatthelandscapescale. Ongoing
climatic chan ges may further acce ntuate this necessit y. Hence, we highlig hted the
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1 | INTRODUCTION
Disturbances are an essential component of forest dynamics that
significantly affect forest biodiversity and species composition
(Schelhaasetal.,2003; Svobodaetal.,2014).Innaturalforests,the
varyingspatialandtemporalextentofdisturbancesandtheirseveri-
tiescreateamosaicofforestswithalternatingstructuralcomplexity
throughoutthelandscape (Sommerfeldetal.,2018).There is avast
diversityoftaxa,eachwithitsownoptimaalongforestsuccessional
stages(Hilmersetal.,2018;Winteretal.,2015),dependingonmicro-
climateandresourceavailability(Bässleretal.,2010).Underachang-
ingclimate,naturaldisturbances, such asbark beetleoutbreaksand
windthrows,arepredictedtoincreaseinextentandfrequency(Seidl
etal., 2014;Sommerfeldetal., 2018). Therefore,itis crucialto un-
derstandthedynamicsofspeciescommunitiesinforestecosystems
shapedbynaturaldisturbanceregimes(Jandaetal.,2017).Although
ourunderstandingoftheeffectsofdisturbancesoncommunitiesof
differ ent groups of fores t organisms has i mproved in recent yea rs
(Mikoláš etal., 2017;Thom&Seidl, 2016; Thornetal.,2019),infor-
mationonthelong-termeffectsofdisturbancesonsomespecialised
taxa,suchaslichens,islacking.
Naturaldisturbancescreatebiological legacies of various quality
for lichens ashabitats. Windstorms usuallycause stems to break or
groups of tr ees to topple over, whe reas trees ki lled by bark bee tles
remainasstandingdeadwoodunt iltheycollapseyear slater.Thesedis-
turbancelegacieschange over timethroughprocessesinfluenced by
thesuccessionalstageofthesurroundingforest.Forexample,asdead-
wooddecomposes,itchangesitsform(Bunnelletal.,2008)thus,over
time, it provides different substrate quality for many lichen species.
Sun-exposedlivetre es,an otherdi sturbanceleg acy,alsoprovideanim-
por tanthabitatformanylichenspecies(Ellis,2012).Therefore,itisnot
onlydeadwoodquantityandquality,butalsotheproportionoflegacy
trees post disturbance that may play a crucial role in maintaining the di-
versityandresilienceofforestcommunities(Zemanováetal.,2017).In
addition,biologicallegaciesoftenserveasthestartingpointforcom-
munity reorganisation after passing ecological bottlenecks (Lõhmus
etal.,2017). Lichenised fungiare goodindicatorsofhabitatcontinu-
ityandthenaturalnessofforests(Bochetal.,2013;Dymytrovaetal.,
2018)becauseoftheirdispersallimitation(Ellis,2012)andnichespe-
cialisationonoldtrees (Williams & Ellis,2015)or deadwood (Bunnell
etal., 2008).However, their response todisturbancesmay vary sig-
nificantly. For example, epiphytic lichens are sensitive to changes in
microclimate thuscanopyremovalcan lead to local die outof some
species (Snäll etal., 2005), whereas other lichen species can benefit
fromincreasedlightlevelsandsubstrateavailability(Ellis,2012).
Recent research indicates that forest succession is nonlinear
andfollowsdeterministicpathwaysconnectingdisturbancehistory
andstructuralcomplexity(Donato et al.,2012;Meigsetal.,2017).
Understandingtheinfluenceofpastdisturbances,currentstructure
and subst rate character istics on lichen diversit y in natural fores t
ecosystems can help to better integrate lichen conservation into
forest management planning. However, to our knowledge, lichen
species r ichness and comp osition across gr adients of natur al dis-
turbanceseverity and history inmulti-ageforestshaverarely been
studied(Hilmersetal.,2018;Johansson,2008).
Toaddress this knowledgegap, we surveyed lichen communi-
tiesinprimaryspruceforestsoftheWesternCarpathians,aregion
drivenbyamixed-severitydisturbanceregime(Jandaetal.,2017).
Based on the dendrochronological reconstruction of the occur-
rence and s everity of dist urbances in t hese stan ds over the past
250 years , we tested how dist urbances have af fected curr ent li-
chenspec ies ric hne ssa ndc omp osition .Wea d dre sse dthefo llo win g
hypotheses:
1. The localenvironment, forest structure and disturbance history
influence lichen diversity at both the object (trees and logs)
and plotlevel.Specifically,we expected that: (a) recentcanopy
removal in the past two decades promotes overall diversity
owing to increased light levels and substrate occupancy by
generalist species, but n ot red-listed and old-grow th specialist
species; (b) with time since disturbance, diversity of all, red-
listed and old- growth specialists increases until deadwood has
decomposed and the tree canopy has recovered.
2. Different disturbance legacies, such as standing deadwood,
downedlogsorremnanttrees,representspecific microhabitats
that host specialised lichen communities.
2 | METHODS
2.1  |  Study area and plot selection
Weselected10primaryspruceforeststandsfromanexistinginven-
toryoftheprimaryforestsofSlovakia(Mikolášetal.,2019;REMOTE
project:www.remoteforests.org/project.php).Thestandsrangedin
sizefrom100to300haandwereselectedfromalandscapeofap-
proximately4,800km2acrossfivemountainrangesintheWestern
Carpathians(Figure1).Owingtothedifferentsizesofthemountain
rangesandtheavailabilityofprimaryforestfragments,weassigned
fourstandstotheHighTatrasregion,twoineachoftheGreatFatra
needtoprotectthelastremainingprimaryforeststoensurethesurvivalofregionally
uniquespeciespoolsoflichens.
KEYWORDS
barkbeetle,deadwood,dendrochronology,forestcontinuity,lichenisedfungi,mixed-severity
disturbanceregime,Picea abies,WesternCarpathians
   
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and Low Tatras regions, and one in each of the Poľana and Pilsko
regions(detailsinAppendixS1).
The bedrock varies from acidic to basic minerals, although
acidic be drock dominates i n the study area . The overall clima te
is cold and wet across all the plots with respective mean annual
temperaturerangingfrom1.6to3.4°Candmeanannualprecipita-
tionrangingfrom1,205to1365mm/year.Treespeciescomposi-
tioncomprisesmorethan90%Picea abies(Norwayspruce),witha
varyingadmixtureofSorbus aucuparia,andtolesserdegrees,Pinus
cembra,Salix caprea,Betula pendula,Fagus sylvatica and Acer pseu-
doplatanus.The distance between the stands ranged from 10to
50km.Primaryforests,unalteredbyhumans,allowedustostudy
disturbanceeffectswithoutconfoundinganthropogenicfactors.
Ineachstand, studyplotswereselectedtocover the wholegradi-
ent of disturbanceseverities andtimingover thepast 250 years. For
thispurpose,wesplitplotsfromJandaetal.(2017)accordingtodistur-
bance event timing into threeequallylarge classes. We thenselected
two plot s within each c lass on every s tand, with d iffering s everity if
available.Theminimumdistancebetweenplotswassetto300mwithin
eachstand.Ofthe60plotsselected,3hadtobeexcludedbecausethey
wereinaccessibleafterseverewindthrowthus,wesampled57plotsin
10standsforanalyses.
2.2  |  Lichen survey and diversity indices
In2017and2018,allepiphyticandepixyliclichens,includingincon-
spicuous microlichens, were recorded on selected objects within
eachcircular plot (1,000 m2) by an ex perienced li chenologis t. We
selectedfiveobjectsoneachplot, whichincluded two livingtrees,
FIGURE 1 Studyarea:the10studiedstandsin5mountainranges.Allstudyplotswereconsideredtobeprimaryspruceforestwithout
substantial human intervention in the past several centuries
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twodownedlogsando nest andingdeadtreeorsnag.Ifaty peofob-
jectdidnotoccurwithintheplot,wesubstituteditwithanobject(s)
ofthemostfrequenttypetomaintainfiveobjectsperplot.Inaddi-
tion,weselecteduptofourotherobjectsinrelationtothesubstrate
variability(e.g.,admixturedtreespecies,deadwoodobjectsinalter-
nativestagesofdecay) to cover theentirerangeof substrate vari-
abilitywithineachplot.Lichenswererecordedonanareafromthe
stembaseuptoaheightof2mforstandingobjectsand2malong
downedlogs,beginning atthelarge end oftheobject.Eachrecord
wasappendedbyabundanceclasses:(a)onetothreethalli,(b)four
toninethalliand(c)morethanninethalli.Lichensontheground,on
rocks or on fallen twigswere not sampled. Alllichens wereidenti-
fiedtothespecieslevelofthefungalcomponenteitherinthefield
or under a mi croscope in th e laborator y.Th e red list sta tuses for
Slovakia accordingtoIUCNcategoriesinclude extinct orregionally
extinct(EX),criticallyendangered(CR),endangered(EN)andvulner-
able(VU),asborrowed fromPišút et al. (20 01).Non-lichenised as-
comycetes of the genera Arthopyrenia,Arthrorhaphis, Microcalicium
and Thelocarponwereincludedintheanalyses.Alllichenrecordsare
presentedinAppendixS3.
Some lichens (including microlichens) are restricted to well-
preser ved old-growth f orests (Dy mytrova et al. , 2018; Gaspary an
et al., 2018; Mal íček et al., 2019). Fruticose sp ecies (Bryoria spp.,
Evernia divaricata,Hypogymnia bitteri,Usnea spp.) generally require
high air humidity and respond negatively to changes in canopy cover
(Dymytrovaetal.,2018).Basedonpreviousliterature,weidentified
alistof26speciesthataretypicalforold-growthspruceforestsof
theWesternCarpathians(AppendixS2).
We calculated three indices for object diversity: species rich-
ness,speciesrichnessofred-listed(threatened)speciesandspecies
richnessofold-growthspecies(Table1).Attheplotlevel,weusedall
surveyedobjectsandrarefiedspeciesrichnessofalllichenspecies,
red-listedandold-growthspecialiststothesamenumberofobjects
(fiveforeachplot)toaccountfordifferencesinsamplesize(Colwell
etal .,2 012)w hil ema int ain ingthewhol era ngeof sub stra tediversity.
2.3  |  Forest structure and disturbance history
Oneachofthe57plots,wegathereddatarelatedtoourvariablesof
interestattheobjectandplotlevelsbasedonaninventor yofalllive
treeswithdiameteratbreastheight(DBH)≥6cm,andstandingand
lyingdeadwoodwithDBH≥10cm(AppendixS1).Wooddecaystage
was divided into five classes according to Stokland et al. (2012).
However,we pooled freshlydead objects with live trees (Lõhmus
&Lõhmus,2001) and objects inadvancedphasesof decay(decay
stages 4and5)duetothesmall samplesizeoffreshlydead(n =1)
andheavilydecayed(n =5)objects,respectively.
Weusedapreviouslypublished250-yearrecordofdisturbance
history(Janda et al.,2017)toinferrelationships between thevari-
abilityofpastdisturbanceprocessesandcontemporarypatternsof
lichencommunitydiversity.Thesechronologieswerederivedfrom
analyses of temporal patterns in inter-annual tree growth. They
includedtwotypesofcanopyaccessionevents,asdeterminedfrom
radial tree growth patterns: (a) open c anopy recruitme nt – rapid
juvenile g rowth rates in dicating rec ruitment in a ca nopy gap, and
(b)release – abrupt and sustainedincreases in annual treegrowth
indicatingmortalityofaneighbouringcanopytree.Thecorrespond-
ingeventseveritywas definedintermsoftheproportional areaof
treecanopyremovedbythedisturbance,whichwasestimatedusing
regression methods and allometric equations relating the aggregate
present-daysizeoftree responders(individuals withadisturbance
signal)totheoriginalextentofthedisturbance-inducedcanopygap
(Lorime r & Frelich, 1989). For more det ails see Janda e t al. (2017,
2019).
Weusedtheresultingreconstructedtimeseriestoderiveatotal
of three dis turbance-base d metrics th at we hypothesise d may in-
fluencethelichenspeciesassemblages,notwithstandingcontempo-
rary forest structure.Disturbance severity represents thecanopy
area removed by the strongest disturbance event that was detected
inthechronology.Timesincedisturbance was defined as thetime
elapsedfromthemaximumdisturbanceseverityeventthataffected
aplotuntil2003,themostrecentyearusedacrossallchronologies.
We defined di sturbance fre quency as the n umber of events wi th
>15%canopyarearemovalwithintheplotchronology.Thetreering-
based disturbance reconstruction ends 10 years prior to the core
extraction date of the tree rings in 2013 owing to methodological
constraints in their calculation using moving windows.
2.4  |  Statistical analyses
Theinfluenceof foreststructureanddisturbance historyonlichen
species r ichness (Hy pothesis 1) was eva luated using li near mixed-
effectsmodels(LMMs)atboththeobjectandplotlevel.Attheplot
level, the response variable was the rarefied species richness of
all, red-listed or old-growth lichens. Full plot-level LMMs involved
fixed effects of disturbance history and forest structure (Table 1),
andrandomeffectsofthestands.Fullobject-levelLMMsincluded
fixedeffectsofobjectcharacteristics,disturbancehistoryandforest
structure, andrandom effectsofstands andobjectsnestedwithin
stands. Full models were checked for multicollinearity using vari-
anceinflationfactors (VIFs).The forest structural characteristic of
basalarea was excludedfromthemodelstoavoid multicollinearity
problems(VIF>10).TheremainingvariablesshowedVIFvalues< 3
whichiswellbelowtherecommendedthreshold(Quinn&Keough,
2002).Finalmodelswerebuiltusingstepwisebackwardelimination
ofnon-significant fixedeffects (α = 0.05).Residualsofthemodels
werecheckedfornormalityandhomogeneityofvariances.Object-
leveldata onthe threatened (red-listed) speciesrichnesswerelog-
transformedtomeettheassumptions.Statisticalsignificanceofthe
fixedeffectswasassessedusingFtestswithSatterthwaite’sapprox-
imationofdegreesoffreedom(Kuznetsovaetal.,2017).Likelihood
ratiotestswereusedtoevaluatesignificanceoftherandomeffects
andtheoverallmodels (Pinheiro &Bates,2000).Marginal(
R2
m
)and
conditional(
R2
c
)determinationcoefficientswerecalculatedforeach
   
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LMMtoquantifytheproportion ofthe totalvariance explained by
thefixedeffectsandbybothfixedandrandomeffects,respectively
(Nakagawaetal.,2017).Tocomparetherelativeimportanceofindi-
vidualvariables,wecalculatedstandardisedregressioncoefficients
(β) and semi-partial marginal determination coefficients (
s
R
2
m
) ob-
tainedfromavariancedecomposition(Stoffeletal.,2021).
Weperformed indicator species analysis (Dufrêne & Legendre,
1997) to evaluate the association of individual lichen species to
predefined disturbance legacies (Hypothesis 2), which are repre-
sentedbydifferentsubstratetypes(livetree,standingdeadtreeor
downedlog)ofthetwomostfrequenthosttreespecies(Picea abies,
S. aucuparia).The indicator value (IndVal) was combinedfrom two
components:specificityandfidelity.Specificityisthenumberofthe
speciesrecordsassociatedwithatargetsubstrate(biologicallegacy),
divided bythe numberoftotal records. Fidelityis the relative fre-
quencyof the speciesassociatedwith atargetsubstrate.Weanal-
ysedeachcombinationofthethreesubstratetypeswithinthehost
treespecies.The significanceof theIndValswas evaluatedusing a
randomisation test. The randomisation scheme was restricted to
10,000free permutations of individualsubstrates within the plots
butnopermutationsamongtheplotstokeeptheeffectoftheplot
constant(Anderson&terBraak,2003).
All analyses were conductedin R (version 3.5.1, RCore Team,
RFoundationforStatistical Computing,Vienna,AT).Speciesasso-
ciations to biological legacies were evaluatedusing the R package
indicspecies(version1.7.4.;RCoreTeam,RFoundationforStatistical
Computing,Vienna,AT).LMMswerefittedwiththelmer-functionin
the lme4package(version1.1-23;Batesetal.,2015),andVIFswere
calculated with the car package (version 3.0-8; Fox & Weisberg,
2019).Weusedtheggplot2package(Wickham,2016)tocreatethe
effectplotsofLMMs. The partR2package(version0.9.1)wasused
forthecalculationofconditionalandmarginal(partial)(function
partR2;Stoffeletal.,2021).
3 | RESULTS
3.1  |  Lichen species diversity and substrate
association
Werecorded158lichenspecies of65generaon479surveyedob-
jectson57plots(Appendix S3). AccordingtotheSlovakianredlist
ofthreatened species, we found 3 species considered extinct(EX;
Usnea scabrata,Lecidea huxariensis,Fellhanera bouteillei),20critically
TABLE 1 Descriptionofdisturbancehistory,foreststructuralanddiversityvariables
Variable Description Unit
Lichencharacteristics
Speciesrichness Numberofrecordedlichenspecies
Threatenedspeciesrichness NumberofthreatenedlichensaccordingtotheredlistofSlovakia(Pišút
etal.,2001)
Old- growth specialists species richness Speciesrichnessofoldgrowth-dependentlichens(Dymytrovaetal.,
2018;Gasparyanetal.,2018;Malíčeketal.,2019)
Substratecharacteristics
Host tree species Host tree species identity Picea abies or Sorbus aucuparia
Substratetype Substrate(object)type:livetree,standingdeadtree,downedlog
Substratesize Diameteratbreastheight(DBH)forliveandstandingdeadtreesor
diameterofthethickerendofdownedlog
mm
Disturbance history
Disturbance severity Canopyarearemovedinthemostsevereeventinthechronology %
Disturbancefrequency Numberofdisturbanceevents>15%canopyarearemoved
Timesincedisturbance Timeelapsedfromtheeventyearto2003 Yea rs
Foreststructure
Livetreedensity Livetreedensity(>60mmDBH) Nu mbe r/ha
Standingdeadtreedensity Standingdeadtreedensity(>60mmDBH) Numb er/h a
Livetreesize MeanDBHoflivetreesontheplot(>60mmDBH) mm
Standingdeadtreesize MeanDBHofstandingdeadtreesontheplot(>60mmDBH) mm
Livetreesizevariability StandarddeviationofDBHofalllivetreesontheplot(>60mmDBH) mm
Standingdeadtreesizevariability StandarddeviationofDBHofallstandingdeadtreesontheplot
(>60mmDBH)
mm
Basalareaoflivetrees Basalarea(BA)oflivetrees(>60mmDBH) m2/ha
Basalareaofstandingdeadtrees Basalareaofstandingdeadtrees(>60mmDBH) m2/ha
Volumeofdownedlogs Volumeofdownedlogsestimatedviaatruncatedcone m3/ha
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endangered (CR), 9 endangered (EN) and 8 vulnerable (VU)lichen
species.Thefivemostfrequentthreatenedlichensinourstudyhad
more than 100 records: Bryoria capillaris (CR), Bryoria fuscescens
(VU), Hypogymnia farinacea(VU),Mycoblastus sanguinarius(CR) and
Parmeliopsis hyperopta(VU).Aquarterofalloccurrenceswerecon-
sidered to be threatened species.
Ofthe158recorded lichens,35exhibited asignificant associa-
tionwithoneorseveraldisturbancelegacytypes(AppendixS4).The
largest group of 19 species was associated with live and standing
deadspruce trees,while11specieswereassociated with hosttree
species S. aucuparia.There werenolichenspecies significantly as-
sociatedspecificallywithstandingdeadtreesandlivesprucetrees,
respectively.
3.2  |  Species richness in relation to the forest
structure and disturbance history
At the plot level, total and red-listed lichen species richness in-
creasedwithmeanstandingdeadtreesize,butdecreasedwithdis-
turbanceseverity(Figure2a,b;Table2).Thenumberofold-growth
specialistswassupportedbythevariabilityinstandingdeadtreesize
andtimesincedisturbances(Table2).
Attheobjectlevel,substratetype,substratesizeand,toalesser
extent, host species, time since disturbance and density of live
trees played significant roles in drivingthe total number of lichen
species (Table 2). The number of speciesincreased with substrate
sizeand timesince disturbance, and decreasedwith livetree den-
sity (Figure 2). Standing live and deadtreeshosteda similar num-
berofspecies,whereasthelichendiversityofthedownedlogswas
significantly lower.Consideringthehost species, sprucesupported
ahigher number of species thanS. aucuparia,althoughsome rarer
species(Bacidia subincompta,Biatora globulosa,Buellia disciformis and
Rinodina orculata)wererecorded onlyon the stemsof S. aucuparia.
The diver sity of red-listed sp ecies was signif icantly infl uenced by
thesamesetofvariablesastotalrichness,exceptforlivetreeden-
sity(Figure2c–f).Finally,thediversityofold-growthspecialistswas
signific antly influe nced by object s ize, object t ype and time sin ce
disturbances(Table2).
4 | DISCUSSION
4.1  |  Lichen communities in disturbance regimes
Wedemonstrated that natural disturbances significantly influence
lichen species diversity and composition in forest ecosystems.
Thisfinding indicates thatchanges in disturbanceregimes caused
byclimatechange(Sommerfeldet al.,2018)will likely affect lichen
communities. Understanding the effectsof different types ofdis-
turban ces is therefore cr ucial for effe ctive conser vation of liche n
communities,particularlyfortheconservationofendangeredlichen
species,whichform asubstantial partofthelichen speciespool in
theWesternCarpathians.
Weshowedthatamixed-severitydisturbanceregime(Jandaetal.,
2017)affectsspeciesrichnessand composition of lichenised fungi.
Lichens,aslong-livedanddisturbance-sensitiveorganisms,seemed
tobe influencedby the disturbance historyof sites. Epiphytic and
epixylic species constitute a patch-tra ckingm etapopulation struc-
tureinwhichpatchappearance(suitablemicrohabitatswithfavour-
ablelightand moistureconditions)underliespotentialcolonisation,
whereas patchdestruction(e.g., treefall) cancauselocal extinction
(Snälletal.,2005).Ontheonehand,severecanopyremovaldisrupts
thecontinuityofmicrohabitatsandmicroclimate,whichmightneg-
ativelyaffectlichencommunities.Ontheotherhand,severedistur-
bancesaltersubstratediversityandincreaselightavailability,which
mightsupportspeciesrichnessintheearlyrecoveryperiodafterthe
di s tur bance ( B u n n e l l e tal.,20 0 8 ).Af teradisturbancee v e n t , t r e e d e n -
sity and c anopy cover increase over time until the habitat achieves
maturity,whichdecreaseslightavailabilityundercanopiesandtends
toreducethespeciesrichnessoflichens(Hilmersetal.,2018;Marini
et al., 2011). Conse quently, severe dis turbances of ten cause, wit h
delay,localextinctionofspecieswithnarrow habitatniches(dueto
their patch-tracking metapopulation structure). By contrast, plots
affectedatmostbysmallgapdynamicsorintermediateratesofcan-
opyremovalinthepastexhibitedspecies-richcommunities,includ-
ingnumerous threatenedlichens.Hence, theresultsprovidesome
evidence that lichen diversit y at the plot scale is promoted according
totheintermediate-disturbancehypothesis(Roxburghet al., 2004).
However,cumulativelichen diversity atabroader landscape scale
likelycoincides with habitat heterogeneity,which points to mixed-
severitydisturbancehypothesis(Mikolášetal.,2017;Thom&Seidl,
2016).Longtemp oralcontinuit yandhighmutua lconne cti vityofhet-
erogeneous habitats can provide a more or less constant availability
ofspecificand/oruniquemicrohabitatsacrossthelandscape, such
aslargedeadwood,aswellas deadwoodinvariousstagesofdecay
(Ellis,2012;Johanssonetal.,2012).
Asa resultofspatio-temporaldisturbance dynamicsandcon-
sequent patch-tracking metapopulation dy namics oflichen spe-
cies, species turnoveralong successional stages on a local scale
(temporal variability inspecies composition) can be comparable
with spatial dissimilarity in species composition at the landscape
scaleinagivensnapshot(Hilmerset al., 2018).However,thisas-
sumptionisrelevantonlyforlandscapesthatencompasssufficient
area ofpri mar yfo res t sinva rio ussucces siona lst age sth atcanpro -
vide the continual appearance of suitable habitatsforall lichens
inalandscapespeciespool.Inthisstudy,wereliablydocumented
robustandlong-termeffectsofdisturbanceregimesontheoccur-
rence of rarelichens.InEuropeanlandscapes wherenaturalfor-
estsarefragmented(Sabatinietal.,2018)and/orthedisturbance
regimeismodifiedbyhumans(Mülleretal.,2019),the(transient)
absence of suitable habitats often leads to species extinction
(Rybickietal.,2020; Snälletal.,2005).Furthermore, themagni-
tudeofspeciesdeclinemayberelativelyinconspicuousforalong
   
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timeowingtospeciessurvivalinextinctiondebt(Dullingeretal.,
2013;Öckinger&Nilsson,2010).Wedonotknowenoughregard-
ing what par t of lichen dive rsity is doo med to extin ction in the
current la ndscape conf iguration an d management an d the addi-
tionaleffectofclimatechange.Inourstudy,localspeciesrichness
peakedinplot ssubjectedtolessseveredisturbancethatoccurred
aratherlongtimeago.Althoughincre asingdis turbancefrequency
andseverityasanaccompanyingeffect ofclimatechangeissup-
posedtobegenerallybeneficialforforestbiodiversity,increasing
thesizeofdisturbedareascan have anegativeeffect,especially
intheEuropeanlandscapewithstaticandspatiallylimitedconser-
vationareas thatrepresenthotspotsofforestbiodiversity(Seidl
etal.,2017;Thometal.,2017).
4.2  |  Lichen species and biological legacies
Inte rmsofhabitatpre fer enc es,nos peciesino urs urveyw ass tric t ly
foundononlylivesprucetrees.Ingeneral,standingdeadtreesand
livetreessharedacommonpoolofspecies.Naturalforestdynam-
icscanleadtodeadwood-dominatedstagesofforestdevelopment
(Zeppenfeld et al., 2015) and thus some species have adapted
andexpandedtheirniches to include both liveandstanding dead
trees.Thesimilarityin lichenspecies compositionbetweendead
andlivespruce treesislikelybecausebark usuallystays on atree
post-dea th,durin gt hee arlya ndintermediates tagesofdec ay.Bar k-
dwelling li chens on live tr ees may, therefore, r emain on the ba rk
oftheobjectafter death(e.g., standingdead trees, downedlogs).
Other sp ecies can colonis e exposed sapwood of the same d ead
tree s.T her efore ,itislikelythatw ew ouldf indam oresp eci ficli che n
community associated with standing dead trees if wefocusedon
alreadydebarkeddeadtrees.Also,aftertheneedleshavedropped,
increased light levels may contribute to the slightly increased spe-
ciesrichnessoflichensonstandingdeadtreescomparedwithlive
trees(Marinietal.,2011).
Downed logs were a unique legacy type; not only were they a
habitat for endangered deadwood spe cialists, such as Xylographa
spp.,butthey also hostedadistinctcommunityoflichens. Despite
lower lichen species richness on downed logs compared with stand-
ingdeadorlivesprucetrees,thespeciespoolsizeoflogswascom-
parablewiththepoolofstandingdeadandlivetrees,whichsuggests
ahigherspeciesturnoverbetweendownedlogs.Weattributedthis
FIGURE 2 Significantdriversofred-listedspeciesrichnessidentifiedatthescaleofplots(a,b)andindividualobjects(c–f).Rarefied
speciesrichness(plot-levelscale)andspeciesrichness(object-levelscale)predictedbythelinearmixedmodels(lines,dots)isdisplayedalong
with95%confidencelimits(greyshading,errorbars).ForthemodeldetailsseeTable2
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toa greater variabilityin substrate conditions on downed logs for
lichens,whichmaybeinfluenced bystageof decomposition,shad-
ing by the sur rounding tree an d herb vegetation , and alternating
groundcontactandwoodmoisturecontentalongitslength(Bunnell
etal.,2008).Studiedprimaryforestsaremostlypuresprucestands,
but the predominant admixture species is the light-demanding
TABLE 2 Summaryoffinalplot-levelandobject-levelmixedmodelsoflichenspeciesrichness(total,old-growthandred-listed)involving
significantfixedeffectsandrandomeffects(re)ofstandsandplotsnestedwithinstands
β (SE)/τ2df F/χ2p- value
s
R
2
m
Significance
Plot- level scale
Totalspeciesrichness[
𝜒2
(3)
=23.4,p <0.0001,
R2
m
=0.328,
R2
c
= 0.412]
Meanstandingdeadtreesize 0.333(0.116) 1/51.1 8.3 0.0058 0.085 **
Disturbance severity −0.388(0.116) 1/51 .9 11.1 0.0016 0.127 **
Stand(re) 3.292 11.1 0.2973 n.s.
Threatenedspeciesrichness[
𝜒2
(3)
=20.6,p =0.0001,
R2
m
=0.228,
R2
c
= 0.412]
Meanstandingdeadtreesize 0.262(0.115) 1/4 8 .5 5.2 0.0269 0.059 *
Disturbance severity −0.341(0.116) 1/49. 3 8.7 0.0049 0.102 **
Stand(re) 1.801 15.9 0.0156 *
Old-growthspecialistsspeciesrichness[
𝜒2
(3)
=27.7,p <0.0001,
R2
m
=0.176,
R2
c
=0.528]
Standingdeadtreesizevariability 0.234(0.099) 1/4 7.1 5.6 0.0222 0.043 *
Timesincedisturbance 0.341(0.097) 1/46.3 12.2 0.0010 0.101 **
Stand(re) 1.810 114.4 0.0001 ***
Object- level scale
Totalspeciesrichness[
𝜒2
(8)
=297.8,p <0.0001,
R2
m
=0.425,
=0.552]
Substratesize 0.313(0.037) 1/4 49.2 73.0 <0.0001 0.086 ***
Hosttreespecies(S. aucuparia)−0.181(0.038) 1/443 .8 24.7 <0.00 01 0.021 ***
Substratetype(standingdeadtree) 0.028(0.038) 2/4 32 . 8 78.0 <0.0001 0.14 4 ***
Substratetype(downedlog) −0.401(0.038)
Livetreedensity −0.186(0.064) 1/51. 5 8.5 0.0052 0.037 **
Timesincedisturbance 0.118(0.058) 1/54.6 4.1 0.0466 0.008 *
Stand(re) 1.862 11.9 0.1628 n.s.
Plot(stand)(re) 4.947 124.4 <0.0001 ***
Threatenedspeciesrichness[
𝜒2
(7)
=111.2,p <0.0001,
R2
m
=0.251,
R2
c
=0.394]
Substratesize 0.241(0.050) 1/3 4 7. 2 23. 2 <0.0001 0.147 ***
Hosttreespecies(S. aucuparia)−0.150(0.044) 1/330.4 14.5 0.0 002 0.025 ***
Substratetype(standingdeadtree) −0.002(0.050) 2/3 29.1 31.1 <0.0001 0. 210 ***
Substratetype(downedlog) −0.353(0.049)
Timesincedisturbance 0.166(0.062) 1/50.8 7.2 0.0099 0.030 **
Stand(re) 0.313 13.1 0.0778 n.s.
Plot(stand)(re) 0.519 19.0 0.0028 **
Old-growthspecialistsspeciesrichness[
𝜒2
(6)
=60.8,p <0.00 01,
R2
m
=0.144,
R2
c
= 0.338]
Substratesize 0.279(0.052) 1/311.9 29.1 <0.0001 0.075 ***
Substratetype(standingdeadtree) 0.086(0.054) 2/296.4 9. 5 <0.0001 0.046 ***
Substratetype(downedlog) −0.169(0.052)
Timesincedisturbance 0.164(0.070) 1/50.9 5.5 0.0227 0.027 *
Stand(re) 0.261 13.8 0.0522 n.s.
Plot(stand)(re) 0.389 110.3 0.0014 **
Notes: Forfixedeffect s,standardisedmodelcoefficients(β)andtheirstandarderrors(SE)aredisplayedalongwiththeteststatistics(F),approximate
degreesoffreedom(dfnumerator/denominator),probabilities(p-value)andsemi-partialmarginaldeterminationcoefficients(
s
R
2
m
).Coefficientsof
categoricalpredictors(hostspecies,substratetype)representdifferencesbetweenagivenlevelofthepredictoranditsbaselevel(hostspecies
–spruce,substratetype–livetree).Fortherandomeffects,estimatesofthevarianceamongstandsandamongplotswithinstandsaregiven(τ2)
withthelikelihoodratioteststatistics(χ2),degreesoffreedom(df )andprobabilities(p-value).Summarystatisticsaredisplayedforeachmodelin
squaredbrackets.Statisticalsignificanceofthemodelparametersisassignedasfollows:non-significant,n.s.(p≥0.05);*p <0.05;**p < 0.01; and
***p < 0.001.
   
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S. aucuparia,whichusuallyoccursingapsorafterlargerdisturbances,
and is shaded out during succession. S. aucupariahasasp eci fic lichen
community,includingseveralthreatenedspecies(e.g.,Biatora efflo-
rescens,Graphis scr ipta)thathasalreadybeendocumentedinCentral
Europe(Malíčeketal.,2019).
4.3  |  Management implications
Theremnantsofprimarymountainforestshaveahighconserva-
tionvalueasdocumentedbythehighfrequencyanddiversityof
red-listedlichenspecies inthis study.Theyarerefuges for three
regi onallyexti nctspec ies andhos tatle ast10%oftheentireli che n
flora of Slovakia (Guttová etal., 2013). Natural disturbances ap-
peartoplay an essential roleinmaintainingthisbiodiversity.To
ensurethesurvivaloflichenspecieswithnarrowhabitatrequire-
ments,it iscriticaltoensurethecontinualpersistenceofforests
inalldevelopmentalphases(Johanssonetal.,2012).Downedlogs
andstandingdeadwoodwereinhabited bydifferentlichencom-
munitie s and are crucia l for the surv ival of a number of l ichens
(Bunnelletal., 2008).Toprotectlichendiversity,we recommend
that no woo dy biomass, live tre es or deadwood, s hould be ex-
tractedfromprimaryforestfragments(inagreementwithMüller
etal.,2019).
The species diversity associated with the primary forests can,
however, decline a s the result of ex tinction d ebt and/or negative
consequencesoftheedgeeffec t,evenifalltheremainingremnants
of the prim ary forest s are protecte d (Berglund & Jo nsson, 2005;
Robergeetal.,2011).Hence,forestsadjacenttotheprimaryforest
remnantsshouldalsobeexcludedfromsalvageloggingtoincrease
habitatareaandlimitpotentialedgeeffectsforthesevaluablefor-
estfragments. When planning conservation measures, we should
takeintoaccount that onlynatural disturbancescanprovidepath-
waysfortheestablishmentofrareand endangered speciesacross
the landscape through legacy formation and structural enhance-
mentofman agedstand s( ssler&Müller,2010;Thornetal .,2019).
ACKNOWLEDGEMENTS
MSvi was supported by the Operational Programme Integrated
Infrastructure(OPII),fundedbytheERDF(ITMS313011T721).
AUTHOR CONTRIBUTIONS
TL propos ed the original id ea for this manuscr ipt, conducte d the
preliminary statistical analyses and wrote the first draft. JHo pro-
gressed,completedandrevisedthemanuscript.JHaconductedthe
lichensurveyandidentifiedthesamplesbyspecies.MSvicarriedout
thefinalstatisticalanalyses.Allauthorscontributedtothewritingof
themanuscript.TLandJHocontributedequallytothiswork.
DATA AVAILAB ILITY STATEMEN T
Thedataofalllichenspeciesrecordsthatsupportthefindingsofthis
study are available in the supplementary materials.
ORCID
Jeňýk Hofmeister https://orcid.org/0000-0002-3915-5056
Marek Svitok https://orcid.org/0000-0003-2710-8102
Martin Mikoláš https://orcid.org/0000-0002-3637-3074
Radim Matula https://orcid.org/0000-0002-7460-0100
Josef Halda https://orcid.org/0000-0002-0264-8535
Václav Pouska https://orcid.org/0000-0003-0388-6065
Ondrej Kameniar https://orcid.org/0000-0002-5653-9457
Daniel Kozák https://orcid.org/0000-0002-2622-370X
Pavel Janda https://orcid.org/0000-0003-4732-6908
Vojtěch Čada https://orcid.org/0000-0002-3922-2108
Radek Bače https://orcid.org/0000-0001-6872-1355
Michal Frankovič https://orcid.org/0000-0003-2772-3738
Ondřej Vostarek https://orcid.org/0000-0002-0657-0114
Miroslav Svoboda https://orcid.org/0000-0003-4050-3422
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SUPPORTING INFORMATION
Additionalsupportinginformation may be found in theonlinever-
sionofthearticleatthepublisher’swebsite.
Appendix S1.Environmentalandstructuralattributesofthestands
and plots.
Appendix S2.Listofold-growthlichenspecies.
Appendix S3.Listofrecordedlichenspeciesinthestandswithindi-
cationoftreespeciesandsubstratesoccupied.
Appendix S4.Listoflichenspeciessignificantlyassociatedwiththe
disturbancelegacies(hosttreespeciesandtype),theirredliststatus,
thenumberofincidencesinthesurvey,andindicatorvalue(IndVal).
How to cite this article:Langbehn,T.,Hofmeister,J.,Svitok,M.,
Mikoláš,M.,Matula,R.,Halda,J.,etal(2021)Theimpactof
natural disturbance dynamics on lichen diversity and
compositioninprimarymountainspruceforests.Journal of
Vegetation Science,32:e13087.https://doi. or g/10.1111/
jvs.130 87
... Over the last decades, due to the global increase in the Earth's temperature, the ecological significance of the spruce bark beetle Ips typographus (L.) infestations have increased in forests including Norway spruce Picea abies (L.) (Fahse & Heurich 2011, Marini et al. 2017, Jakoby et al. 2019, Netherer et al. 2021. Massive outbreaks of this cambiofagous beetle, indigenous in the spruce forests of Europe, constitute a natural phenomenon conditioning the dynamics of these forests (Čada et al. 2016(Čada et al. , Langbehn et al. 2021. As a result, they contribute to the formation of gaps filled in by snags in the forest stand. ...
... Due to stand disturbance, both groups benefit from the possibility of spreading to surfaces free of competing organisms and from increased access to light , Kharpukhaeva & Mukhortova 2016. For the epiphytes that slowly retreat from the bark remnants, the ability to inhabit the wood gives them a chance to survive (Kushnevskaya & Shorohova 2018, Langbehn et al. 2021. ...
... At the same time, the species diversity of all of the ecological groups of the wood-inhabiting lichens was greater than that found on the bark. Recently, similar results were reported by Langbehn et al. (2021), who showed that all the epiphytic species found on living trees around disturbed areas in Carpathian forests, expanded their niches on the decaying wood. ...
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Tanona M., Czarnota P., 2022. What determines the diversity and succession of lichens inhabiting post-bark beetle snags in the Western Carpathians? Ann. For. Res. 65(1): 65-84. Abstract The life strategy of Norway spruce allows the recovery of European spruce forests in a scenario of catastrophic disturbances caused by the European spruce bark beetle. However, little is known about how the development of this insect infestation has influenced the preservation of the ecological balance in these forests over the last decades. Based on the upper montane spruce forests in the Polish Western Carpathians, we decided to check what species of lichens are using the decaying wood of post-bark beetle snags and how the progressive changes in wood hardness and stand decomposition affect the process of species exchange. In 2018-2019, we investigated spruce snags on permanent monitoring plots in Gorce National Park, whose cause and time of death have been recorded since 1999, and earlier in 1992 and 1997. The study covered 374 post-bark beetle spruce snags at 76 sites. We found 84 species, including 77 lichens, 6 lichenicolous fungi and one non-lichenised fungus, 15 of which were exclusively wood-inhabiting species in Gorce range. Using generalised linear models, the wood age (A) and the scale of the forest stand breakdown phenomenon (B) were compared with the altitude (C), the aspects of hillside exposure (D) and the forest plant community (E) in the assessment of their effect on lichen species diversity and abundance. "A" was the most important of the tested factors, significantly and positively influencing both parameters, while "B-D" only weakly influenced lichen abundance. Five groups of wood age, significantly different in the lichen abundance and the composition of species were distinguished, and a characteristic combination of dominant species was determined for each of them. Based on the measurements of the wood hardness under the thalli using Shore's method, the succession of species during the colonisation of the post-bark beetle snags was determined and four groups of species were selected, most frequent in the successive stages of wood decay process. The wood of spruces killed by the bark beetle is both an important substrate enabling the survival of obligately wood-inhabiting lichen species, as well as providing a habitat supporting the maintenance of epiphytes in the Carpathian forests. This study extends the knowledge about the specific requirements of lichens inhabiting spruce snags, as well as the pace and course of lichen succession on this substrate.
... Primary forests are essential refuges for biodiversity, including many endemics and species of high conservation value (Moning & Müller, 2009;Wallenius et al., 2010;Paillet et al., 2015;Eckelt et al., 2018;Di Marco et al., 2019;Langbehn et al., 2021), but due to omnipresent historic land use, they are incredibly rare in Europe (Parmasto, 2001;Sabatini et al., 2020). Since ancient times, these forests were used for acquisition of pastures through deforestation, fuel wood and timber extraction. ...
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Understanding the processes shaping the composition of assemblages at multiple spatial scales in response to disturbance events is crucial for preventing ongoing biodiversity loss and for improving current forest management policies aimed at mitigating climate change and enhancing forest resilience. Deadwood-inhabiting fungi represent an essential component of forest ecosystems through their association with deadwood decomposition and the cycling of nutrients and carbon. Although we have sufficient evidence for the fundamental role of deadwood availability and variability of decay stages for fungal species diversity, the influence of long-term natural disturbance regimes as the main driver of deadwood quantity and quality has not been sufficiently documented. We used a dendroecological approach to analyse the effect of 250-years of historical natural disturbance and structural habitat elements on local (plot-level) and regional (stand-level) species richness of deadwood-inhabiting fungi. We used data collected from 51 study plots within nine best-preserved primary spruce forest stands distributed across the Western Carpathian Mountains. Historical disturbances shaped the contemporary local and regional species richness of fungi, with contrasting impacts of disturbance regime components at different spatial scales. While local diversity of red-listed species has increased due to higher disturbance frequency, regional diversity of all species has decreased due to higher severity historical disturbances. The volume of deadwood positively influenced the species richness of deadwood-inhabiting fungi while canopy openness had a negative impact. The high number of observed rare species highlights the important role of primary forests for biodiversity conservation. From a landscape perspective, we can conclude that the distribution of species from the regional species pool is-at least to some extent-driven by past spatiotemporal patterns of disturbance events. Natural disturbances occurring at higher frequencies that create a mosaic forest structure are necessary for fungal species-especially for rare and endangered taxa. Thus, both the protection of intact forest landscapes and forest management practises that emulate natural disturbance processes are recommended to support habitats of diverse fungal communities and their associated ecosystem functions.
... The impact on epiphytic lichens of forest exploitation, ecological conditions in edge fragments of forests and remnants of old stands has been repeatedly studied (Esseen and Renhorn, 1998;Kivistö and Kuusinen, 2000;Hilmo and Holien, 2002;Rheault et al., 2003;Nascimbene et al., 2013). On the other hand, studies of changes in the epiphytic lichen biota generated by the natural forest dynamics, including those created by natural disturbances, have so far been rarely undertaken (McCune et al., 2008;Bartels and Chen, 2015;Langbehn et al., 2021). ...
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Over the last decades the West Carpathian spruce and mixed forests with a share of Picea abies, have been undergoing intensified dynamic changes, determined by windstorms and European spruce bark beetle outbreaks. Those changes should have a decisive effect on the survivability of species and shifts in epiphytic lichen communities on this phorophyte. Research conducted in the Gorce Mts (West Carpathians, Poland) in 1993, 2013 and 2018, on the same 186 spruce trees at 33 sites, revealed an increase in the species diversity of lichen communities in a long-term perspective (25 years). At the same time, there was a decrease in the coverage of the dominant species. Such changes are a result of long-term tree composition processes: the natural thinning of upper mountain spruce forests and the increase of lower mountain forests density after a decrease in the share of Norway spruce. The former prefers photophilous epiphytes, and the latter leads to an increase in the share of shade-tolerant species. The analysis of lichen communities by means of the principal components analysis (PCA) method for all three study periods combined showed that long-term changes were the most significant for this lichen biota, and short-term changes had no considerable effect. The conducted Redundancy Analysis (RDA) revealed, that the forest plant association was a stronger factor affecting the lichen community composition and coverage than tree stand density and saplings density in each observation term. The changes taking place in stands under bark beetle and wind disturbances should be treated differently in different types of forest associations, but in both, they cause differentiation of niches used by more specialized species of epiphytic lichens. Full article available to download by URL Share Link https://authors.elsevier.com/c/1ey36,Q4YJXeD8
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Aim Primary forests have high conservation value but are rare in Europe due to historic land use. Yet many primary forest patches remain unmapped, and it is unclear to what extent they are effectively protected. Our aim was to (1) compile the most comprehensive European‐scale map of currently known primary forests, (2) analyse the spatial determinants characterizing their location and (3) locate areas where so far unmapped primary forests likely occur. Location Europe. Methods We aggregated data from a literature review, online questionnaires and 32 datasets of primary forests. We used boosted regression trees to explore which biophysical, socio‐economic and forest‐related variables explain the current distribution of primary forests. Finally, we predicted and mapped the relative likelihood of primary forest occurrence at a 1‐km resolution across Europe. Results Data on primary forests were frequently incomplete or inconsistent among countries. Known primary forests covered 1.4 Mha in 32 countries (0.7% of Europe’s forest area). Most of these forests were protected (89%), but only 46% of them strictly. Primary forests mostly occurred in mountain and boreal areas and were unevenly distributed across countries, biogeographical regions and forest types. Unmapped primary forests likely occur in the least accessible and populated areas, where forests cover a greater share of land, but wood demand historically has been low. Main conclusions Despite their outstanding conservation value, primary forests are rare and their current distribution is the result of centuries of land use and forest management. The conservation outlook for primary forests is uncertain as many are not strictly protected and most are small and fragmented, making them prone to extinction debt and human disturbance. Predicting where unmapped primary forests likely occur could guide conservation efforts, especially in Eastern Europe where large areas of primary forest still exist but are being lost at an alarming pace.
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Given the global intensification of forest management and climate change, protecting and studying forests that develop free of direct human intervention-also known as primary forests-are becoming increasingly important. Yet, most countries still lack data regarding primary forest distribution. Previous studies have tested remote sensing approaches as a promising tool for identifying primary forests. However, their precision is highly dependent on data quality and resolution, which vary considerably. This has led to underestimation of primary forest abundance and distribution in some regions, such as the temperate zone of Europe. Field-based inventories of primary forests and methodologies to conduct these assessments are inconsistent; incomplete or inaccurate mapping increases the vulnerability of primary forest systems to continued loss from clearing and land-use change. We developed a comprehensive methodological approach for identifying primary forests, and tested it within one of Europe's hotspots of primary forest abundance: the Carpathian Mountains. From 2009 to 2015, we conducted the first national-scale primary forest census covering the entire 49,036 km 2 area of the Slovak Republic. We analyzed primary forest distribution patterns and the representativeness of potential vegetation types within primary forest remnants. We further evaluated the conservation status and extent of primary forest loss. Remaining primary forests are small, fragmented, and often do not represent the potential natural vegetation. We identified 261 primary forest localities. However, they represent only 0.47% of the total forested area, which is 0.21% of the country's land area. The spatial pattern of primary forests was clustered. Primary forests have tended to escape anthropogenic disturbance on sites with higher elevations, steeper slopes, rugged terrain, and greater distances from roads and settlements. Primary forest stands of montane mixed and subalpine spruce forests are more abundant compared to broadleaved forests. Notably, several habitat types are completely missing within primary forests (e.g., floodplain forests). More than 30% of the remaining primary forests are not strictly protected, and harvesting occurred at 32 primary forest localities within the study period. Almost all logging of primary forests was conducted inside of protected areas, underscoring the critical status of primary forest distribution in this part of Europe. Effective conservation strategies are urgently needed to stop the rapid loss and fragmentation of the remaining primary forests. Our approach based on precise, field-based surveys is widely applicable and transferrable to other fragmented forest landscapes.
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Disentangling the importance of developmental vs. environmental drivers of variation in forest biomass is key to predicting the future of forest carbon sequestration. At coarse scales, forest biomass is likely to vary along major climatic and physiographic gradients. Natural disturbance occurs along these broad biophysical gradients, and depending on their extent, severity and frequency, could either amplify or dampen spatial heterogeneity in forest biomass. Here we evaluate spatial variation in the basal area of late-successional Picea abies (L./Karst.) forests across the Carpathian Mountain Range of central Europe and compare the roles of coarse-scale biophysical gradients and natural disturbances in driving that variation across a hierarchy of scales (landscapes, stands, and plots). We inventoried forest composition and structure, and reconstructed disturbance histories using tree cores collected from 472 plots nested within 30 late-successional stands, spanning the Carpathian Mountains (ap-proximately 4.5 degrees of latitude). We used linear mixed-effects models to compare the effect of disturbance regimes and site conditions on stand basal area at three hierarchical scales. We found that the basal area of late-successional Picea abies forests varied across a range of spatial scales, with climatic drivers being most important at coarse scales and natural disturbances acting as the primary driver of forest heterogeneity at fine scales. For instance, the stand-level basal area varied among landscapes, with the highest values (48-68 m 2 ha −1) in the warmer southern Carpathian Mountains, and lower values (37-52 m 2 ha −1 on average) in cooler areas of the eastern and western Carpathians. Finer-scale variation was driven by local disturbances (mainly bark beetle and windstorms) and the legacies of disturbances that occurred more than a century ago. Our findings suggest that warming could increase the basal area of northern sites, but potential increasing disturbances could disrupt these environmental responses.
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European landscape conservation includes the recognition of inter-related ‘ancient’ and ‘old-growth’ woodland. Ancient woodland is defined by its temporal continuity, which can be measured through its consistent occurrence on historic maps over a period of time, typically several centuries. Old-growth woodland has attributes of both temporal continuity and structural complexity; European old-growth woodland is now extremely rare and a valuable conservation resource. Indicator species provide recognition of old-growth woodland, through traits that are sensitive to its defining features: (i) dispersal limitation demanding temporal continuity of suitable habitat prior to colonisation (as is associated with ancient woodland), and/or (ii) specialist niches associated with old and senescent trees (which may or may not be found in ancient woodland, depending on its past management). To test the response of indicators to each of these features, niche models were developed for lichen epiphytes in an ancient and structurally diverse woodland stand, thus corresponding to ‘old-growth’ condition. Models were projected for the ancient and an adjacent regenerated stand. There was less suitable habitat in the regenerated stand, and a lower proportion of suitable habitat was occupied. Nevertheless, indicators had colonised from the ancient to the regenerated stand within 50 years. Viewed against the background of previous work, we conclude that landscape context - the spatial relationship between ancient and regenerated woodland - is critical to the interpretation of indicators, which are perhaps better conceptualised as markers of threat and conservation value than independent measures of woodland history.