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Arthropod communities in fungal fruitbodies are weakly structured by climate and biogeography across European beech forests

DOI:10.1111/ddi.12882
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Nicolas Friess
Nicolas Friess
Nicolas Friess
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Jörg Müller at University of Wuerzburg
Jörg Müller
Pablo Aramendi
Pablo Aramendi
Pablo Aramendi
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Claus Bässler at Nationalpark Bayerischer Wald
Claus Bässler
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Abstract and Figures

Aim The tinder fungus Fomes fomentarius is a pivotal wood decomposer in European beech Fagus sylvatica forests. The fungus, however, has regionally declined due to centuries of logging. To unravel biogeographical drivers of arthropod communities associated with this fungus, we investigated how space, climate and habitat amount structure alpha and beta diversity of arthropod communities in fruitbodies of F. fomentarius. Location Temperate zone of Europe. Taxon Arthropods. Methods We reared arthropods from fruitbodies sampled from 61 sites throughout the range of European beech and identified 13 orders taxonomically or by metabarcoding. We estimated the total number of species occurring in fruitbodies of F. fomentarius in European beech forests using the Chao2 estimator and determined the relative importance of space, climate and habitat amount by hierarchical partitioning for alpha diversity and generalized dissimilarity models for beta diversity. A subset of fungi samples was sequenced for identification of the fungus’ genetic structure. Results The total number of arthropod species occurring in fruitbodies of F. fomentarius across European beech forests was estimated to be 600. Alpha diversity increased with increasing fruitbody biomass; it decreased with increasing longitude, temperature and latitude. Beta diversity was mainly composed by turnover. Patterns of beta diversity were only weakly linked to space and the overall explanatory power was low. We could distinguish two genotypes of F. fomentarius, which showed no spatial structuring. Main conclusion Fomes fomentarius hosts a large number of arthropods in European beech forests. The low biogeographical and climatic structure of the communities suggests that fruitbodies represent a habitat that offers similar conditions across large gradients of climate and space, but are characterized by high local variability in community composition and colonized by species with high dispersal ability. For European beech forests, retention of trees with F. fomentarius and promoting its recolonization where it had declined seems a promising conservation strategy.
Map of the 61 sampling sites of this study. The green area depicts the predicted current distribution of European beech Fagus sylvatica (Brus et al.., 2011). The numbers in the map correspond to the study site ID in supporting information Appendix S2 and Appendix S3: Table S3.1. Circles indicate the 52 study sites for which data on all arthropods were available; squares indicate the nine sites for which only beetle data were available and which are part of the analyses in Supporting information Appendix S4. Black filling indicates sites with active forest management and white filling indicates unmanaged sites. Left inset: A typical example of a European beech tree with fruitbodies of Fomes fomentarius. Photograph by Thomas Stephan. Right inset: Mean annual temperature and annual precipitation of all study sites (filled circles and squares (see above)) and 10,000 randomly sampled points in the distribution of F. sylvatica representing the climate space where beech‐dominated forests are occurring
Map of the 61 sampling sites of this study. The green area depicts the predicted current distribution of European beech Fagus sylvatica (Brus et al.., 2011). The numbers in the map correspond to the study site ID in supporting information Appendix S2 and Appendix S3: Table S3.1. Circles indicate the 52 study sites for which data on all arthropods were available; squares indicate the nine sites for which only beetle data were available and which are part of the analyses in Supporting information Appendix S4. Black filling indicates sites with active forest management and white filling indicates unmanaged sites. Left inset: A typical example of a European beech tree with fruitbodies of Fomes fomentarius. Photograph by Thomas Stephan. Right inset: Mean annual temperature and annual precipitation of all study sites (filled circles and squares (see above)) and 10,000 randomly sampled points in the distribution of F. sylvatica representing the climate space where beech‐dominated forests are occurring
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Pie chart of the proportion of species from different arthropod orders reared from fruitbodies of Fomes fomentarius from 52 beech‐dominated forest sites across Europe. The overall number of determined species was 216
Pie chart of the proportion of species from different arthropod orders reared from fruitbodies of Fomes fomentarius from 52 beech‐dominated forest sites across Europe. The overall number of determined species was 216
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Rank‐incidence plot of all 216 arthropod species reared from fruitbodies of Fomes fomentarius from 52 beech‐dominated forest sites across Europe
Rank‐incidence plot of all 216 arthropod species reared from fruitbodies of Fomes fomentarius from 52 beech‐dominated forest sites across Europe
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Relative contribution of predictor sets in explained deviance of alpha and beta diversity and its components turnover and nestedness. Alpha diversity was modelled using generalized linear models and the relative contribution is based on hierarchical partitioning. Beta diversity is based on presence–absence data and its components were modelled using generalized dissimilarity models and the relative contribution was calculated as the “pure” effect of the predictor set on the overall explained deviance of the model. All analyses were conducted for all species and fungi specialists separately and for the trophic levels consumer, predator and parasitoids. Bar colours represent the predictor sets with space in black, climate in light grey, habitat amount in white and the deviance shared by the predictors in dark grey
Relative contribution of predictor sets in explained deviance of alpha and beta diversity and its components turnover and nestedness. Alpha diversity was modelled using generalized linear models and the relative contribution is based on hierarchical partitioning. Beta diversity is based on presence–absence data and its components were modelled using generalized dissimilarity models and the relative contribution was calculated as the “pure” effect of the predictor set on the overall explained deviance of the model. All analyses were conducted for all species and fungi specialists separately and for the trophic levels consumer, predator and parasitoids. Bar colours represent the predictor sets with space in black, climate in light grey, habitat amount in white and the deviance shared by the predictors in dark grey
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Relationship between (a) the number of arthropod species per fruitbody sample and sample size, that is the total weight of the 10 sporocarps sampled, of 52 sites and (b) the number of beetle species per fruitbody sample and sample size including all 61 sites. Circles indicate the 52 study sites for which data on all arthropods were available; squares indicate nine sites for which only beetle data were available and which are part of the analyses in Supporting information Appendix S4. Black filling indicates sites with active forest management, white filling indicates unmanaged sites. A simple regression line and confidence interval are shown. Axes are log‐transformed
Relationship between (a) the number of arthropod species per fruitbody sample and sample size, that is the total weight of the 10 sporocarps sampled, of 52 sites and (b) the number of beetle species per fruitbody sample and sample size including all 61 sites. Circles indicate the 52 study sites for which data on all arthropods were available; squares indicate nine sites for which only beetle data were available and which are part of the analyses in Supporting information Appendix S4. Black filling indicates sites with active forest management, white filling indicates unmanaged sites. A simple regression line and confidence interval are shown. Axes are log‐transformed
… 
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Diversity and Distributions. 2019;25:783–796. wileyonlinelibrary.com/journal/ddi 
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 783
Received:23April2018 
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  Revised:18O ctober2018 
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  Accepted:11November2 018
DOI:10.1111/ddi.12882
BIODIVERSITY RESEARCH
Arthropod communities in fungal fruitbodies are weakly
structured by climate and biogeography across European beech
forests
Nicolas Friess1 | Jörg C. Müller2,3  | Pablo Aramendi4 | Claus Bässler2 | 
Martin Brändle1 | Christophe Bouget5 | Antoine Brin6 | Heinz Bussler7 | 
Kostadin B. Georgiev2,3 | Radosław Gil8 | Martin M. Gossner9 | 
Jacob Heilmann‐Clausen10 | Gunnar Isacsson11 | Anton Krištín12 | Thibault Lachat13,14 | 
Laurent Larrieu15,16 | Elodie Magnanou17,18  | Alexander Maringer19 | Ulrich Mergner20 | 
Martin Mikoláš21,22 | Lars Opgenoorth1 | Jürgen Schmidl23 | Miroslav Svoboda21 | 
Simon Thorn3 | Kris Vandekerkhove24 | Al Vrezec25 | Thomas Wagner26 | 
Maria‐Barbara Winter27 | Livia Zapponi28 | Roland Brandl1 | Sebastian Seibold29
1DepartmentofEcology‐AnimalEcology,FacultyofBiology,Philipps‐UniversitätMarburg,Marburg,Germany
2BavarianForestNationalPark,Grafenau,Germany
3FieldStationFabrikschleichach,DepartmentofAnimalEcologyandTropicalBiology,UniversityofWürzburg,Biocenter,Rauhenebrach,Germany
4Vermungsgade,Copenhagen,Denmark
5Irstea,'ForestEcosystems'ResearchUnit,Nogent‐sur‐Vernisson,France
6INPT–Ecoled'IngénieursdePurpan,UMR1201DynaforINRA‐INPT,UniversityofToulouse,Toulouse,France
7AmGreifenkeller1b,Feuchtwangen,Germany
8DepartmentofEvolutionary,BiologyandEcology,InstituteofInvertebrateBiology,FacultyofBiologicalSciences,UniversityofWroclaw,Wrocław,Poland
9ForestEntomology,SwissFederalResearchInstituteWSL,Birmensdorf,Switzerland
10CenterforMacroecology,EvolutionandClimate,NaturalHistoryMuseumofDenmark,UniversityofCopenhagen,Copenhagen,Denmark
11SwedishForestA gency,Hässleholm,Sweden
12InstituteofForestEcolog ySAS,Zvolen,Slovakia
13SchoolofAgricultural,ForestandFoodSciencesHAFL,BernUniversityofAppliedSciences,Zollikofen,Switzerland
14SwissFederalResearchInstituteWSL,Birmensdorf,Switzerland
15INRA ,UMR1201DYNAFOR ,ChemindeBordeRouge,UniversityofToulouse,CastanetTolosanCedex,France
16CRPFOC ,Tolosane,France
17SorbonneUniversités,UPMCUnivParis06,CNRS,BiologieIntégrativedesOrganismesMarins(BIOM),Banyuls/Mer,France
18Réser veNaturelleNationaledelaForêtdelaMassane,Argelès‐sur‐Mer,France
19GesäuseNationalPark,Admont,Austria
20ForestCompanyEbrach,Ebrach,Germany
21FacultyofForestryandWoodSciences,CzechUniversityofLifeSciencesPrague,Prague,CzechRepublic
22PRALES,Rosina,Slovakia
23Ecologygroup,DevelopmentalBiolog y,DepartmentBiology,UniversityofErlangen‐Nuremberg,Erlangen,Germany
24ResearchInstituteforNatureandForestINBO,Geraardsbergen,Belgium
25NationalInstituteofBiology,Ljubljana,Slovenia
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,
providedtheoriginalworkisproperlycited.
©2019TheAuthors.Diversity and DistributionsPublishedbyJohnWiley&SonsLtd.
784 
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     FRIESS Et al.
26Depar tmentofBiolog y,UniversityofKoblenz‐Landau,Koblenz,Germany
27ForestResearchInstituteofBaden‐Würt temberg(FVA),Freiburg,Germany
28CentroNazionaleperloStudioelaConservazionedellaBiodiversitàForestale"BoscoFontana",Marmirolo,Italy
29TerrestrialEcolog yResearchGroup,DepartmentofEcologyandEcosystemManagement,TechnischeUniversitätMünchen,Freising,Germany
Correspondence
SebastianSeibold,TerrestrialEcology
ResearchGroup,Depar tmentofEcology
andEcosystemManagement,Technische
UniversitätMünchen,Freising,Germany.
Email:sebastian.seibold@tum.de
Funding information
RudolfandHeleneGlaserFoundation;
MinisterstvoŠkolství,Mládežea
Tělovýchovy,Grant/AwardNumber:CZ.0
2.1.01/0.0/0.0/16_019/0000803;Česká
ZemědělskáUniverzitavPraze,Grant/
AwardNumber:CIGANo.20184304
Editor:AnnaTraveset
Abstract
Aim:ThetinderfungusFomes fomentariusisapivotalwooddecomposerinEuropean
beechFagus sylvaticaforests.Thefungus,however,hasregionallydeclinedduetocen‐
turiesoflogging.Tounravelbiogeographicaldriversofarthropodcommunitiesassoci‐
atedwiththisfungus,weinvestigatedhowspace,climateandhabitatamountstruc ture
alphaandbetadiversityofarthropodcommunitiesinfruitbodiesofF. fomentarius.
Location:TemperatezoneofEurope.
Tax o n:Arthropods.
Methods:Werearedarthropodsfromfruitbodiessampledfrom61sitesthroughout
therangeofEuropeanbeechandidentified13orderstaxonomicallyorbymetabar‐
coding.WeestimatedthetotalnumberofspeciesoccurringinfruitbodiesofF. fom en‐
tarius in European beech forests using the Chao2 estimator and determined the
relativeimportanceofspace,climateandhabitatamountbyhierarchicalpartitioning
foralphadiversityandgeneralizeddissimilaritymodelsforbetadiversity.Asubsetof
fungisampleswassequencedforidentificationofthefungus’geneticstructure.
Results:ThetotalnumberofarthropodspeciesoccurringinfruitbodiesofF. fomentarius
acrossEuropeanbeechforestswasestimatedtobe600.Alphadiversityincreasedwith
increasingfruitbodybiomass;itdecreasedwithincreasinglongitude,temperatureand
latitude. Beta diversitywas mainly composed by turnover.Patterns of beta diversity
wereonlyweaklylinkedtospaceandtheoverallexplanatorypowerwaslow.Wecould
distinguishtwogenotypesofF. fomentarius,whichshowednospatialstructuring.
Main conclusion: Fomes fomentariushost s a l a r g e n u m b er o f a r th ro p o ds i n Eu r o p e a n
beechforests.Thelowbiogeographicalandclimaticstructureofthecommunities
suggeststhatfruitbodiesrepresentahabitatthatoffers similarconditionsacross
largegradientsofclimateandspace,butarecharacterizedbyhighlocalvariability
incommunitycompositionandcolonizedbyspecieswithhighdispersalability.For
European beech forests, retention of trees withF. fomentariusandpromotingits
recolonizationwhereithaddeclinedseemsapromisingconservationstrategy.
KEY WORDS
deadwood,Fagus sylvatica,Fomes fomentarius,insects,invertebrates,restoration,saproxylic,
sporocarp
1 | INTRODUCTION
Most parts of the temperate zone of Europe—from the Iberian
Peninsula to the Black Sea and from southern Italy to southern
Sweden—are naturallycoveredby forestsdominated by European
beechFagus sylvatica (Fig ure 1). These forests, however,have de‐
clined over recent centuries due to deforestation until around
1800,andsincethenduetoconversiontoconifer‐dominated(Pinus
sylvestris,Picea abies)plantations(Dirkx,1998;Schelhaas,Nabuurs,&
Schuck,2003).Historicdeforestationanddegradationhaverecently
been reinforced by large‐scale clear‐cutting of old‐growth beech
forestsin regionsthat,until recently, were rather unaffected (e.g.,
intheCarpathians;Vanonckelen&VanRompaey,2015;Mikolášet
al.,2017).Sincethe distributionofEuropean beechisrestricted to
thetemperatezoneofEurope,theEUhas acknowledgeditsglobal
responsibilitybylistingseveraltypesofbeechforestasNatura2000
    
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FRIESS E t al.
habitats(CounciloftheEuropeanUnion,).Furthermore,someofthe
lastnaturaloralmostnaturalEuropeanbeechforestsarepartofthe
UNESCO World Heritage “Ancient and PrimevalBeech Forests of
theCarpathians andOther RegionsofEurope”(http://whc.unesco.
org/en/list/1133).Despitethesecommitmentstoconservingbiodi‐
versityinEuropeanbeechforests,ourunderstandingoflarge‐scale
driversof biodiversity inbeechforests remainslimited,hampering
systematic conservation planning, given prevalent area conflicts
(Ammeretal.,2018;Kouki,Hyvärinen,Lappalainen,Martikainen,&
Similä,2012;Margules&Pressey,2000).
ThespeciespooloforganismsassociatedwithEuropeanbeech
forestscanbeexpectedtobestructuredacrosslargespatialscales
reflecting different underlying mechanisms. European beech was
one of the last tree species to recolonize central and northern
EuropefromitsmajorrefugiainsouthernEuropeafterthelastgla‐
ciation and is still expandingits range towards the north andeast
(Magri, 2008). Understorey plant diversity in European beech for‐
estsreflectsthishistoryandisdeterminedbydistancetothenear‐
estknownmajorrefuge(Jiménez‐Alfaroetal.,2018;Willner,Pietro,
&Bergmeier,2009).Inaddition,populationsofEuropeanbeechmay
alsohavepersistedinmicrorefugiaincentralEurope(Robin,Nadeau,
Grootes,Bork,&Nelle,2016).Duetoitshighcompetitivenessand
climate tolerance,Europeanbeech covers a widerange of climatic
conditions (Figure 1; Brunet, Fritz, & Richnau, 2010), which might
structurecommunities(Heilmann‐Clausenetal.,2014).Towardsits
ecologicalrangelimits,increasingpresenceofothertreespeciesand
arthropodsassociatedtothesetrees (Brändle&Brandl,2001)may
furtherinfluencetheregionalspeciespool.
These natural drivers ofcommunity structure in beech forests
interact with anthropogenic factors. Forest clearing and forest
manageme nt have been more intens e in western than in e astern
Europeresultinginagradientofhabitatlossofnaturalbeechforest
and conse quently fragme ntation of these fo rests from eas t–west
(Abrego,Bässler,Christensen, & Heilmann‐Clausen, 2015;Kaplan,
Krumhardt, & Zimmermann,2009;Larsson,2001). Manyspecialist
speciesforold‐growthbeechforestshavethusbecomerarerorlo‐
callyextinctinwesternEuropeandcantodayonlybefoundineast‐
ernEurope(Eckeltetal.,;Speight,1989).
Onsmallerspatialscales,speciescommunities canbe affected
bytheregionalclimate acting as environmental filterasshown for
wood‐inhabitingbeetlesandfungiinbeechforests(Bässler,Müller,
Dziock,&Brandl,2010;Mülleretal.,2012)andminutetree‐fungus
beetlesinfruitbodies(Reibnitz,1999).Moreover,notonlylarge‐scale
gradients of anthropogenic pressure can influence communitiesin
FIGURE 1 Mapofthe61samplingsitesofthisstudy.ThegreenareadepictsthepredictedcurrentdistributionofEuropeanbeech
Fagus sylvatica(Brusetal..,2011).ThenumbersinthemapcorrespondtothestudysiteIDinsupportinginformationAppendixS2and
AppendixS3:TableS3.1.Circlesindicatethe52studysitesforwhichdataonallarthropodswereavailable;squaresindicatetheninesites
forwhichonlybeetledatawereavailableandwhicharepartoftheanalysesinSupportinginformationAppendixS4.Blackfillingindicates
siteswithactiveforestmanagementandwhitefillingindicatesunmanagedsites.Leftinset:AtypicalexampleofaEuropeanbeechtree
withfruitbodiesofFomes fomentarius. PhotographbyThomasStephan.Rightinset:Meanannualtemperatureandannualprecipitationof
allstudysites(filledcirclesandsquares(seeabove))and10,000randomlysampledpointsinthedistributionofF.sylvaticarepresentingthe
climatespacewherebeech‐dominatedforestsareoccurring
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beech forests butalsothe amountofavailablehabitat at localand
landscapescales(Fahrig,2013;Seiboldetal.,2017)andtheconnec‐
tivityofhabitat patches (Abrego et al., 2015; Nordén et al.,2018;
Rukke,2000).
Fun giareth emainbiot icagent sofwooddecom posit ionan dt heir
myceliaandfruitbodiesareanimportantfoodformanyarthropods
astheycontain higherconcentrationsofnutrientsstoredin amore
ac ces sibl efor mtha ninundec ayed woo d(Fi lipi ak,S obczyk, &Weine r,
2016;Merrill&Cowling,1966;Stokland,Siitonen,&Jonsson,2012).
Inparticular,fungalfruitbodies,especiallypolypores,serveashabi‐
tatformany fungicolousarthropod species(Schigel,2012).Studies
ofthediversityandcompositionoffungicolousarthropodcommuni‐
tieshavesofarbeenrestrictedtolocalandregionalscales,andgen‐
erallyindicatethatmanyarthropodspeciesarehost‐specific(Jonsell
&Nordlander,2004;Komonen,2001).Occurrenceandabundanceof
fungicolousarthropodspeciesonsingletreesandforeststandsde‐
pendonhabitatavailability(Rukke,2000).Attheregionalscale,turn‐
overinspeciescompositionhasbeenfoundtobehighamongfungal
host spe cies, but low amon g sites across host sp ecies (Komonen,
2001).Sofar,nostudyhasinvestigateddiversitypatternsoffungic‐
olousarthropodsatcontinentalscales(Schigel,2012).
ThetinderfungusFomes fomentariusisoneofthemaindecom‐
posersofwoodinmanybeechforestsinEurope.However,F. fomen‐
tarius has a much l arger range tha n European bee ch covering the
temperate and boreal zones of Europe, Asia and Nor th America.
Outsidebeechforests,itoccursespeciallyinriparianandborealfor‐
estsonBetula,Populus, Alnus orotherhardwoodtrees(Matthewman
&Pielou,1971;Reibnitz,1999;Rukke,2000).Asawhite‐rotfungus,
itcan efficiently break down lignocellulose andcontributes tothe
death ofweakenedliving trees, thus promoting naturalforest dy‐
namics(Butin,1989).Itsfruitbodiesandthecreateddeadwoodare
habitatformanyarthropodspecies (Schigel,2012).Their commu‐
nitycompositionislargelyaffectedbythephysicalconditionsofthe
fruitbodieswhichchangewithongoingdecomposition(Dajoz,1966;
Reibnitz, 1999; Thunes &Willassen, 1997).Thus, in order to cap‐
ture the w hole local com munity occur ring in F. fomentarius differ‐
entstagesofdecompositionhavetobetakenintoaccount(Graves,
1960).
Treescolonized by the fungus have been suggested as afocal
habitat for biodiversity conservation in beech forests (Larrieu
et al., 2018; Mül ler, 2005). Howe ver, due to centuri es of logging
and direct persecution for phytosanitary reasons, populations of
this fungus have declined orbecamelocally extinctin many areas
(Vandekerkhove etal., 2011;Zytynskaet al.,2018). Toguide con‐
servation planning andstrategies inEuropeanbeechforests, such
asthe selectionof areastobe setaside forconservation(Bouget,
Parmain,&G ilg ,2014)orforacti verestoratio nbyde adwoodenrich‐
ment(Dörfler,Gossner,Müller,&Weisser,2017), it isnecessaryto
understandhowarthropodcommunities—whichrepresentthelarg‐
estfractionofanimalbiodiversityinforests—arebiogeographically
structured.
In this study, we reared arthropods from fruitbody samples of
F. fomentarius across the whole distributional range of European
beech.Ouraimsweretoestimatealphaandbetadiversityofarthro‐
podsinfruitbodiesofF. fomentariusandtodise nt angletheeffect sof
post‐glacialrecolonizationofitshosttree,macro‐climate,anthropo‐
genicpressureandhabitatamountondiversitypatterns.Specifically,
weexpected (a) decreasing alphadiversity and increasingnested‐
nesswithlatitudeduetotherecolonizationhistoryofbeech,(b)de‐
creasingalphadiversity and increasing nestednessfromeast‐west
due to the an thropogenic l and use histor y, (c)i ncreasing tur nover
withincreasingdifferencesinmacro‐climaticconditionsacrossboth
latitudinalandlongitudinalspace,and(d)increasingalphadiversity
withincreasinghabitatamountatlocalandlandscapescales.
2 | METHODS
2.1 | Collection of Fomes fomentarius fruitbodies
We collected fruitbodies from 61 beech‐dominated forest sites
across the distributional range of F. sylvatica (Figure 1) between
JuneandAugust2013.Thesesiteswerechosentocoverthenatural
distributionofF. sylvatica,aswellasthefullrangeofclimaticcondi‐
tions withinthis area(Figure1).Wewerenot abletoincludesites
from someparts of thedistributionalrange,for example southern
England,whereF. fomentarius isalmostabsentforhistoricalreasons
(Abreg o, Christensen, B ässler, & Ainswort h, 2017). Sites were lo‐
cated inunmanaged (36) and managed forests (25); both manage‐
mentcategorieswereevenlydistributedacrossEurope(Figure1).
Forarthropodrearing,wecollected10fruitbodiesofF. fomentar‐
iuspersitefoll owi nga stand ardizedpro toc ol.A ssem blagesi nhab iting
fruitbodiesofbracketfungichangewithongoingfruitbodydecom‐
position.Therefore,wesampledfruitbodiesatdif ferentsuccessional
stagesofdecay.Ateachsite,samplingincludedfruitbodiesattached
towoodthathadjustrecentlydiedandwerestillmoist(3to4fruit‐
bodies)andfruitbodiesthathadbeendeadforalongertime(6to7
frui tbodies).Thelatterwer ee itherdrywhens tillatta chedtowoo d(3
to4fruitbodies)orwetwhenlyingontheground(3to4fruitbodies).
Thissamplingprotocolaimedatcoveringmostoftheavailablehab‐
itatheterogeneityrepresentedbythefruitbodies.Thetotalvolume
sampledpersiterangedbetween0.2and21.7kg(mean:2.7kg)and
didnotrepresent the local availabilityoffruitbodies as transporta‐
tionandrearinglogisticsrestrictedthesampledvolume.
In additi on, we collect ed samples of li ving fruitb odies to anal‐
ysethe geneticstructure withinthe population of F. fomentarius in
Europe.Fromthesesamples,weappliedamicrowave‐basedmethod
toextractDNA(Dörnte&Kües,2013)andamplifiedsequencesfor
theinternaltranscribedspacer(ITS)regionandtheelongationfactor
α(efa)genebytouchdownPCR(fordetails,seeSupportinginforma‐
tionAppendixS1).
2.2 | Arthropod rearing
Toreararthropods,allfruitbodiesofthesamesite(fromnowoncalled
“sample”) w ere put into a cardbo ard box (25cm×25cm×50cm)
in an unheated well‐ventilated storage room with a seasonal
    
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FRIESS E t al.
temper ature regime. A tra nsparent collec ting jar was att ached to
eachboxandfilledwith90%ethanoltocollectarthropodsattracted
tolight.Collectingjarswereemptiedeverytwomonthsandarthro‐
podsinside theboxeswerecollectedbyhand. Rearingwascarried
outfor12monthsforeachsample.
2.3 | Arthropod identification and classification
Reared ar thropod specimens were stored in ethanol and beetles
were determined to species level by taxonomists. The remaining
fauna was identified by metabarcoding using next‐generation se‐
quencin g carried out by Adv anced Identific ation Methods G mbH
(Munich,Germany;fordetails,seeSupportinginformationAppendix
S1).Arthropodsequenceswerematched against the publicly avail‐
able DNA barcode library within the Barcode of Life (BOLD—
v4.boldsystems.org; Ratnasingham & Hebert, 2007). Laboratory
problemsimpededtheuseofnext‐generationsequencingforsam‐
plesfromninesites(Figure1).
Weconsideredallspeciesthatwererearedfromfruitbodysam‐
ples,includingspeciesthatusehollowfruitbodiesas shelterorde‐
velopattheinterfacebetweenfruitbodiesandwhite‐rottenwood.
However, since this i ncludes specie s that do not intera ct directly
with the fruitbody, we additionally analysed the data excluding
these species.Basedon literature,we classified species orgenera
thatare knownto feeddirectly on thefungaltissue or exclusively
preyuponmycetophagousspeciesas“fungispecialists”(Supporting
informationAppendixS2);andweclassifiedallspeciesaccordingto
theirtrophiclevelasconsumers(i.e.,speciesthatfeedonnon‐animal
tissue),predators(i.e.,speciesthatfeedonanimaltissue)orparasit‐
oids(i.e.,speciesthatdeveloponorwithinsinglehostorganismsand
ultimatelykilltheirhost).
2.4 | Environmental predictor variables
Coordinatesofeachsitewererecordedin the fieldusinghandheld
GPSdevices(SupportinginformationAppendixS3,TableS3.1).We
extracteddataonall19bioclimaticvariablesforeachsitefromthe
WorldClim database (Hijmans, Cameron, Parra, Jones, & Jarvis,
2005).Sincebioclimaticvariablesareoftencorrelated,weperformed
aprincipalcomponentanalysisonthecorrelationmatrixfortemper‐
atureandprecipitationvariablesseparately(i.e.,temperature:BIO1
–11;precipitation:BIO12–19).Thefirsttwoprincipalcomponents
explainedmostofthevariationinbothdatasets(temperature:75%;
precipitation:91%;SupportinginformationAppendixS3,TableS3.2)
andweresubsequentlyusedasaproxyforbioclimaticconditionsat
thesites.Thefirstprincipal componentsrepresented a gradient in
meantemperatureorprecipitationwithhighvaluesindicatingsites
withoverallhightemperatureorsumsofprecipitation,respectively.
Thesecondprincipalcomponentsrepresentedagradientinseason‐
ality withhigh values forsites displaying hightemperature orpre‐
cipitationseasonality,respectively.
Too btain a proxy f or landscap e‐scale habi tat amount an d an‐
thropogenicpressure,we calculated the proportionofforestcover
surroundingthe sitesforradiifrom 100 to 5,000m(100‐msteps).
Forest coverwithina radiusof700maround siteshadthehighest
independenteffectonalphadiversity,andthus,thisradiuswascho‐
senforfurtheranalyses(SupportinginformationAppendixS3,Figure
S3.1).WeuseddatabasedonLandsatsatelliteimagesfromtheda‐
tabaseonGlobalForestChange(Hansenetal.,2013),whichisavail‐
ablewithaspatialresolutionofapproximately25metresperpixel,
withvaluesrangingfrom0to100perpixelencodingtheproportion
ofcanopyclosureforallvegetationtallerthan5minheight.Toeval‐
uatetheroleofsamplesize(asaproxyforlocalhabitatamount)for
alphaand betadiversity,werecordedthetotal dryweightoffruit‐
bodiespersampleafter12monthsofrearing.Proportionsofforest
coverwerelogit‐transformedandsamplesizewasloge‐transformed.
2.5 | Statistical analyses
AllstatisticalanalyseswerecarriedoutusingR version3.3.2(RCore
Tea m, 2016) .T he main analyses i ncluded beetl es identified t axo‐
nomicallyandallotherarthropodsidentifiedbymetabarcodingand
werethus restricted to the52sites for which metabarcoding data
wereavailable.Additionalanalyseswereconductedforbeetledata
fromall61siteswithbeetleabundances(seeSupportinginformation
AppendicesS4andS5).
Toestimate the overall species pool, we calculated the Chao2
estimator, as implemented in the vegan package version 2.4–3
(Oksan en et al., 2018). The Chao2 es timate is a functi on of spe‐
ciesoccurringonceortwiceinthedatasetandoffersrobustlower
bound es timation for sp ecies richnes s based on inciden ces under
theassumptionthatrarespecieshavesimilardetectionprobabilities
(Chao, 1987). Cal culations were b ased on data for a ll species and
separatelyforfungispecialistsandeachtrophicguild(i.e.,consumer,
predator a nd parasitoid ) on the 52 sites. In ad dition, we use d the
rarefaction–extrapolation framework based onsp eciesincidences
acrossallsites(Chaoetal.,2014).WeusedHillnumberoftheorders
0(species richness),1 (the exponential of Shannon's entropy) and
2(the inverse of Simpson's concentration)to analyse thediversity
ofrare andcommonspecies within one framework. We used 999
replicated bootstraps to calculateconfidence intervalsaround the
species‐accumulationcurves using the iNEXT package (Hsieh, Ma,
&Chao,2016).
Alphadiversitywascalculatedasthenumberofspeciespersite.
Toestimate therelative importance of thepredictor variables, we
performedhierarchicalpartitioning—asimplementedinthehier.part
package version 1.0–4 (Walsh & Mac Nally,2013)—based ongen‐
eralizedlinearmodels.Forthegeneralizedlinearmodels,wechose
aquasipoissonerrordistributionanda log‐linkfunctionin orderto
accountforfrequentlyobservedoverdispersioninmodelsofcount
data.Ple asenotethatalternativelych oosingmod elsincludin ga no b‐
serva tion‐level ran dom effect o rm odels with a neg ative‐binomia l
errordistributiondidnotalterthemainresults.Themodelsincluded
alphadiversity as the dependentvariableandspace(latitude,lon‐
gitude),climate(meantemperature,temperatureseasonality,mean
precipitation,precipitation seasonality)andhabitatamount(forest
788 
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cover,sample size)aspredictor variable sets. Allcalculations were
performedseparatelyforallspecies,fungispecialistsandeachtro‐
phicguildonthe52sites.
BetadiversitywascalculatedastheSørensendissimilarityamong
all 52 sites using presence–absence information. The community
compositionofall speciesandfungi specialistswasvisualized using
non‐metricmultidimensionalscaling(NMDS).Subsequently,wefit‐
tedtheenvironmentalvectorsofspace,climateandhabitatamount
to the resulting ordination as implemented in the envfit function
using the vegan package. In ad dition, we per formed an a nalysis of
similarityin ordertotest for groupdifferences in communitycom‐
position a mong managed and un managed sites, as wel l as among
biogeographicalregionsagainusingvegan (seeSupportinginforma‐
tionAppendixS3forfurtherdetails).Furthermore,wedecomposed
beta diversity in its turnover and nestedness components based
onthe Sørensenindexfamilyas implementedinbetapart (Baselga,
Orme,Villeger,Bortoli,&Leprieur,2017).Theturnovercomponent
representsbetadiversityintroducedbythereplacementofspecies
betweensites,whilethenestednesscomponentrepresentsthebeta
diversityintroducedbytheremoval/gainofspeciesbetweensites.
Toestimatethe relativeimportanceofthepredictor variables (lati‐
tude,longitude, meantemperature,temperatureseasonality,mean
precipitation,precipitationseasonality,forestcoverandsamplesize)
for beta diversity, we calculated generalized dissimilarity models
(GDMs)asimplementedinthegdmpackage(Manionetal.,2017)for
totalbetadiversity,andturnoverandnestednesscomponentssep‐
arately. GDMs allow theanalysis of spatial patternsof community
compositionacrosslargeregions under consideration of nonlinear
relationshipsbetweendissimilarityincommunitycompositionalong
environmentalgradients(Ferrier,Manion,Elith,&Richardson,2007).
AllGDMswerecalculatedusingthedefaultofthree I‐splines.The
calculatedcoefficientfor each of the threeI‐splinesrepresentsthe
rateofchangealongathirdofthegradientoftheenvironmentalpre‐
dictorwhenkeepingallotherpredictorsconstant(i.e.,highvaluesof
thefirstI‐splineindicateahigh rateofchange alongthe first third
ofthegradient).Weestimatedtherelativecontributionofeachpre‐
dictorsetasthedifferenceinexplaineddeviationbetweenamodel
containingallpredictorsetsandamodel fromwhichthispredictor
setwasremoved(Legendre&Legendre,1998;Maestri,Shenbrot,&
Krasnov,2017).Allcalculationswereagainperformedseparatelyfor
allspecies,fungispecialistsandeachtrophicguildonthe52sites.
Dataforbeetlesincludingabundances wereavailable for all61
sites;wethusconductedsimilaranalysesforthisgroupasforallar‐
thropods(seeSupportinginformationAppendicesS4andS5).These
analysesconsideredtheinfluenceofincreasingnumbersofindivid‐
ualsonalpha diversity andtheeffectof space,climate and habitat
amountonabundance‐baseddissimilaritiesofthebeetlecommuni‐
ties. He re, we used Bray–Cur tis dissimil arities and de composed it
intothetwocomponentsbasedonbalancedvariationinabundance
(i.e., individuals of some species ata site are substituted by equal
numbersof individualsat anothersite)and dissimilarityintroduced
byabundancegradients(i.e.,individualsarelostwithoutsubstitution
fromonesitetotheother;Baselga,2013).
3 | RESULTS
In total, we identified 216 arthropod species emerging from fruit‐
bodiesof F. fomentariusfrom52sites.Speciesbelongedto13or‐
ders, with highest species richness found in Diptera ( n=72) and
Coleoptera(n=71;Figure2;SupportinginformationAppendixS2).
The majority oftaxa (n=179) couldbe assigned to species bythe
taxonomist or by alignment of operationaltaxonomic units (OTUs;
see Supporting information Appendix S1)with existing databases.
Theremaining37OTUsnotassignedtoaspeciesweremostlymem‐
bers ofthe Cecidomyiidae (Diptera), for whichbarcodes were not
availableinthedatabases.Weidentified74speciesasfungispecial‐
ists.Concerningtrophicguilds,weclassified131speciesasconsum‐
ers, 68 speciesaspredatorsand17species as parasitoids.Genetic
analysisofF. fomentariussamplesrevealedtwogenotypesthatwere
previouslyidentified aspossiblesympatric crypticspecies(termed
genotype“A”and“B”;Judova,Dubikova,Gaperova,Gaper,&Pristas,
2012).However,intraspecificgeneticvariationamongsiteswasvery
lowandgenotypeBoccurredonlyatfiveofoursiteswidelyspread
overthesamplingarea(SupportinginformationAppendixS1).
Chao2 est imators indic ated an overall s pecies pool of 5 87(S E
=103) for all specie s, 249(S E =181) for fungi spe cialists, 40 2 (SE
=104) for consumer s, 163 (SE =43) fo r predators an d 42(S E =24)
for parasitoids associated with F. fomentarius in European beech
forest s. The observed effec tive number of typical species (q=1)
was87,whilethe observedeffective number of dominant species
(q=2)was 44 (Supporting informationAppendix S3, Figure S3.3).
Manyofthedominantspecieswereconsumers,such as beetles of
the family Ciidae, the Tenebrionidae Bolitophagus reticulatus, the
micro‐mothScardia boletellaandCecidomyiidaesp.3(Figure3).The
most frequent par asitoids were the hyme nopterans Astichus spp.
andascuttlefly(Phoridae).Beetlesincludedfourspeciesconsidered
tobe “primeval forest relicts” (Eckeltet al., ), namely Bolitophagus
interruptus, Bolitochara lucida, Teredus cylindricus and Philothermus
evanescens, whi ch were each found at on e site (Slovenia, France ,
southernItalyandSweden,respectively).
FIGURE 2 Piechartoftheproportionofspeciesfromdifferent
arthropodordersrearedfromfruitbodiesofFomes fomentariusfrom
52beech‐dominatedforestsitesacrossEurope.Theoverallnumber
ofdeterminedspecieswas216
    
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FRIESS E t al.
Consideringallarthropods,themeanspeciesnumberpersite
was16(SE=6) with thelowest number (six species) foundin the
German Wetterauandthe highestnumber(36 species)locatedin
Abruzzo,Italy.Inthequasipoissonmodels,ourpredictorvariables
explained20%ofthedevianceinalphadiversityforallspeciesand
26% for the fung i specialists (F igure 4). The explain ed deviance
decreased from consumers(22%) topredators (16%)and parasit‐
oids(6%)correlatedtothenumberofspeciesofthetrophicguilds
(Table 1).According to hierarchical part itioning, habitat amount,
thatisforestcoverandsamplesize,explainedmostoft hedeviance
inourmodels(Fig ure4).Alp hadiver sit yofa llspecies,fungisp ecial‐
is t s ,cons u mersa n dpred a torsi ncrea s e dwit h incre a sing s amples ize
(Table1,Figure5a)andthatofconsumersalsoincreasedwith in‐
creasingforestcover.Moreover,alphadiversityofallspecies,fungi
specialistsandconsumersdecreasedwithincreasinglongitudeand
thatoffungispecialistsalsodecreasedwithlatitude.Alpha diver‐
sityoffungispecialistsandconsumersadditionallydecreasedwith
increasingmeantemperatureandprecipitation(Table1).Mostef‐
fects,however,wereonlymarginallysignificant(Table1).
Ordinationofthecommunitycompositionofallspeciesas well
asfungispecialistsrevealedlargedifferencesincommunitycompo‐
sition acrossour study sites(Supporting informationAppendixS3:
Figure S3 .2). Except for a si gnificant ef fect of samp le size on the
communitycompositionofallspecies(r2=0.13,p < 0.05), environ‐
mentalvariableswerenotsignificantlycorrelatedwiththeaxesofthe
NMDS(SupportinginformationAppendixS3;FigureS3.2A&D).In
addition,wefoundnodifferencesincommunitycompositionamong
managedandunmanagedsites,aswellasamongbiogeographicalre‐
gions(SupportinginformationAppendixS3:FigureS3.2).Thelargest
proportionofdissimilaritywasduetoturnover,ratherthannested‐
nessforallspecies(98%),fungispecialists(96%)andalltrophicguilds
(consumer:97%;predator:99%;parasitoids:97%).Theproportionof
devianceexplainedbyGDMswasbelow15%foroverallbetadiver‐
sity,nestednessandturnoverinallgroups(Figure4).Forallspecies,
wefoundamarginallysignificantincreaseofdissimilarityintroduced
bynestedness with increasinglongitudinal distance between sites
(Table2).Nosinglepredictorhadasignificanteffectonbetadiver‐
sityoffungispecialists andconsumerspecies (Supportinginforma‐
tionAppendixS3,TableS3.4&TableS3.5).Dissimilarityinlatitudinal
distancehadasignificantpositiveeffectontheoverallbetadiversity
aswellasontheturnovercomponentforpredatorsandparasitoids
(Suppor ting inform ation Append ix S3, Table S3.6 and Table S3 .7).
Additionally,wefoundasignificantincreaseinoverallbetadiversity
aswellasindissimilarityduetoturnoverwithincreasingdissimilarity
ofsamplesizeforpredators.
Our a n a l ysesfo r b e e t l esfroma l l61 sitesi n c l u d e dabundan c e data
for123 species (Supporting information AppendixS5).Here,alpha
diversitywasstronglyaffectedbysamplesize(Figure5;Supporting
informationAppendixS4,TableS4.1).Thenumberofbeetlespecies
increased with fungal sample size as the range in samplesize was
consider ably higher acr oss all 61 sites (Figure 5b) th an across the
subset of 52 sites (F igure 5a). Beetl e community co mposition was
FIGURE 3 Rank‐incidenceplotofall216arthropodspecies
rearedfromfruitbodiesofFomes fomentariusfrom52beech‐
dominatedforestsitesacrossEurope
FIGURE 4 Relativecontributionofpredictorsetsinexplaineddevianceofalphaandbetadiversityanditscomponentsturnoverand
nestedness.Alphadiversitywasmodelledusinggeneralizedlinearmodelsandtherelativecontributionisbasedonhierarchicalpartitioning.
Betadiversityisbasedonpresence–absencedataanditscomponentsweremodelledusinggeneralizeddissimilaritymodelsandtherelative
contributionwascalculatedasthe“pure”effectofthepredictorsetontheoverallexplaineddevianceofthemodel.Allanalyseswere
conductedforallspeciesandfungispecialistsseparatelyandforthetrophiclevelsconsumer,predatorandparasitoids.Barcoloursrepresent
thepredictorsetswithspaceinblack,climateinlightgrey,habitatamountinwhiteandthedeviancesharedbythepredictorsindarkgrey
Parasitoids
Predator
Consumer
Fungi specialists
All species
01020
Alpha diversity
0510 15
Beta diversity
0510 15
Turnover
0510 15
Nestedness
Space
Climate
Shared
Habitat
amount
Explained deviance
in alpha-diversity (%)
Deviance explained exclusively
by sets of variables (%)
790 
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affec ted by dissimilarit y in sample size and longitude. Here, bee‐
tle commu nities showed i ncreased rat es of turnover and balanc ed
changes of abundances withlongitudeand increased ratesofnest‐
ednessandabundancegradientswithsamplesize.Ourmodelsforall
beetle species explainedupto59%of the deviance in alpha diver‐
sity,34% inSørensen dissimilarity and 19%inBray–Curtisdissimi‐
larity(SupportinginformationAppendixS4,TableS4.1;FigureS4.1).
Var iable slinkedtoha bit atamountconsis tentl yexplainedmos toft he
devianceinmodelsofspeciesrichness,overallcommunitycomposi‐
tionandcommunitydissimilarityduetonestedness,whilevariables
linkedtospatialdistanceexplainedmostofthedevianceduetospe‐
ciesturnover(SupportinginformationAppendixS4).
4 | DISCUSSION
Overall,our results indicatethatfruitbodiesof F. fomentariusform
an important micro‐habitat in European beech forests, host inga
rich fauna (estimat ed ~600 art hropod species). Howe ver, t he ar‐
thropod communities included about 30 dominantspecies which
occurredatmost sitesacrossEurope andcan beconsideredtypi‐
cal for fr uitbodies of F. fomentarius. Moreover, there was a lar ge
number of species thatuse F. fomentarius fruitbodiesoccasionally.
The latter groupincludes fungicolousspecies usingawiderrange
offungal hosts (e.g.,Bolitophagus interruptus,Coleoptera,which is
more common on Ischnoderma spp.),speciesthatfeedonwhite‐rot‐
ten wood (e.g ., Corymbia scutellata, Coleoptera) or fu ngal mycelia
and spec ies that use cavi ties inside fru itbodies sim ply for shelter
(e.g. , Amaurobius fenestralis, Aranaea)or that benefit from arthro‐
podprey(e.g.,Plegaderus dissectus, Coleoptera).Alpha diversity in‐
creasedwithsamplesizeanddecreasedwithlongitude,latitudeand
temperature.Despitethelargeextentcoveredinourstudy(approx.
1,80 0km in latitude an d 3,000km in lo ngitude), beta dive rsity—
which wascharacterized by high turnover—wasnot structured by
drivers associated withspace, the biogeographyofF. sylvatica and
habitat amount. Moreover, increasing nestedness and decreasing
TABLE 1 Z‐valuesandexplaineddevianceofgeneralizedlinearmodels(quasipoissonfamily)withthenumberofspeciesofallspeciesor
withinguildsasresponsevariables.Significanteffectsareindicatedbyboldtypesetting.PC1andPC2refertothefirsttwoaxesofthe
respectiveprincipalcomponentanalysesoftemperatureorprecipitationvariables(seeMethodssection)
Predictor set Predictor All species Fungi specialists Consumer Predator Parasitoids
Space Latitude −1.36 −1. 98 ** −1 .70 ** −0.08 −0.93
Longitude −1. 77** −2 .1 2* −1. 8 2** −1 . 0 8 −0.34
Climate Temperature(PC1) −1 .7 2** −1. 90** −1. 92 ** −0.48 −1. 0 0
Temperature(PC2) −0.82 −0.79 −0.43 −1.24 0.31
Precipitation(PC1) −1.41 −1. 3 0 −1. 5 7 −0.68 −0.01
Precipitation(PC2) −0.31 0 .13 −0.45 0.74 −1. 49
Habitatamount Forestcover 1. 26 0.94 1.45 0.13 −0.13
Samplesize 1.75** 2.20*1.55 2.20*0.17
Explaineddeviance 0.20 0.26 0.22 0.16 0.06
Note. aSignificancelevels:*p<0.05,**p < 0.1
FIGURE 5 Relationshipbetween(a)thenumberofarthropodspeciesperfruitbodysampleandsamplesize,thatisthetotalweightof
the10sporocarpssampled,of52sitesand(b)thenumberofbeetlespeciesperfruitbodysampleandsamplesizeincludingall61sites.
Circlesindicatethe52studysitesforwhichdataonallarthropodswereavailable;squaresindicateninesitesforwhichonlybeetledata
wereavailableandwhicharepartoftheanalysesinSupportinginformationAppendixS4.Blackfillingindicatessiteswithactiveforest
management,whitefillingindicatesunmanagedsites.Asimpleregressionlineandconfidenceintervalareshown.Axesarelog‐transformed
(a) (b)
    
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FRIESS E t al.
alpha diversity towards theeast follow not the continental gradi‐
entofincreasinglanduseintensityfromtheCarpathianstowestern
Europe.
Post‐glacial dispersal lags have been identified as one of the
driving mechanisms causing patterns of alpha and beta diversity
acrossEuropeinplants,insectsandvertebrates(Pinkertetal.,2018;
Svenning, Fløjgaard,&Baselga,2011;Svenning,Normand,&Skov,
2008).Incontrast,betadiversityofsaproxylicbeetleswasshownto
behigherbetweensitesthanbetweenelevationalzonesandbiore‐
gions(Mülleretal.,2012).Wefoundonlyaweakdecreaseinalpha
diversityoffungispecialistswithlatitudeandnosignificanteffectof
latitudinaldistanceonbetadiversityofallarthropodsandthetrophic
guildsinF. fomentarius fruitbodies.Onlypredatoryspeciesshowed
an increased rate in turnover with increasing latitudinal distance:
the rateof change in species composition was highest atlow lati‐
tudes (Supportinginformation Appendix S3,TableS3.6).There are
several potentialexplanations as to why post‐glacialrecolonization
ofthemainhost treespecies appears to be ofminor relevance for
communitiesofarthropods occurring inF. fomentariusfruitbodies.
For instance, species associated with fungal fruitbodies ingeneral
displayhighdispersalabilities(Komonen&Müller,2018).Flightmill
experiments showedadispersal ability of Neomida haemorrhoidalis
and Bolitophagus reticulatus(bothColeoptera;bodylength:6–8mm
and 6 – 7.5mm, respectively; Wagner & Gosik, 2016) of>30km
and>100km, respectively (Jonsson, 2003). Additionally, there is
evidence thatthegenetic distance offungivores doesnotincrease
with geographic distance, indicating the absence of dispersal lim‐
itation ( Kobayashi & S ota, 2016). Another poss ible explanatio n is
thatalthough European beechis the mainhost of F. fomentarius in
temperateEuropetoday,otherhoststhatrecolonizedEuropemuch
earlier—suchasbirch—arealsofrequentlyused(Judovaetal.,2012).
IfF. fomentarius recolonizedEuropewiththelattertreespecies,its
arthropods may have had more time for recolonization and thus
post‐glacialdispersallagsarelesslikelytobeimportant.Last,ifmi‐
crorefugiaofEuropeanbeechalsooccurredincentralEurope(Robin
etal.,2016),recolonizationpathwaysmay becomplexandnotwell
describedbylatitudeusedasaproxyfordistancetomajorrefugiain
southernEurope.
TABLE 2 CoefficientsofthreeI‐splines(i.e.,1,2and3)fromtheGDMofoverallbetadiversity,turnoverandnestednessofallarthropod
species.Significant(p < 0.05)ormarginallysignificant(p<0.1)P‐valuesfortheI‐splinesofthepredictorvariablesafter999permutations
areindicatedbyboldtypesettingPC1andPC2refertothefirsttwoaxesoftherespectiveprincipalcomponentanalysesoftemperatureor
precipitationvariables(seeMethodssection)
Response matrix Predictor set Predictor
I‐spline
Sum of
coefficients P1 2 3
Overallbeta Space Latitude 0.155 0.007 0.003 0.165 0 .11
Longitude 00.067 00.067 0.42
Climate Temperature(PC1) 0 0 0 0 0.99
Temperature(PC2) 0.017 0 0 0.017 0.68
Precipitation(PC1) 0 0 0 0 0.99
Precipitation(PC2) 0.061 0 0 0.061 0.35
Habitatamount Forestcover 00.016 00.016 0.73
Samplesize 0.12 0 0 0.1 2 0. 24
Turnover Space Latitude 0.116 00.054 0.170 0 .24
Longitude 0 0 0.082 0.082 0.46
Climate Temperature(PC1) 0 0 0 0 0.99
Temperature(PC2) 0.004 00.030 0.034 0.65
Precipitation(PC1) 0 0 0 0 0.99
Precipitation(PC2) 0 0 0 0 0.99
Habitatamount Forestcover 00.018 0.001 0.019 0.73
Samplesize 0.121 0 0 0.121 0.25
Nestedness Space Latitude 0.001 0 0 0.001 0.70
Longitude 0.132 0 0 0.132 0.07
Climate Temperature(PC1) 0.013 0 0 0.013 0. 51
Temperature(PC2) 0 0 0 0 0.98
Precipitation(PC1) 0.010 0 0 0.010 0.57
Precipitation(PC2) 0.018 0 0 0.018 0.47
Habitatamount Forestcover 0.05 0 0 0.05 0.27
Samplesize 0 0 0 0 0.97
792 
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Agradientofdecreasinganthropogenicpressurefromwesternto
easternEuropeexplainswhymanyspecialistspeciesofold‐growth
forest s have become rar e or extinct i n western Europ e (Eckelt et
al.,;Ódoretal.,2006;Speight,1989).Wethusexpectedtofindan
increase of fungicolous arthropod alpha diversity with increasing
longitu de, but in fac t we observed a we ak decrease . Additionall y,
wefoundamarginallysignificant increaseincompositionaldissim‐
ilarity due to nes tedness with incre asing longitudinal distance of
the overal l arthropo d community. Howeve r,the r ate of change in
compositionduetonestednesswashighestatlowlongitudes,while
explanatory power was low and nestedness did not account for
more than4%of compositionaldissimilarity(Table 2). Forbeetles,
we found an in creased rate in tu rnover and balance d changes of
abundanceatthelowerendofthelongitudinalgradient(Supporting
informationAppendixS4, TableS4.4). In parallel to thegradient of
historicanthropogenicpressure,thereisaneast–westclimaticgradi‐
entfromoceanictowardsmorecontinentalclimates,whichisshown
byamoderatecorrelationbetweenclimatevariablesandlongitude
(Supporting information Appendix S3, TableS3.3). Bothdecreasing
alphadiversityandincreasingnestednesswithincreasinglongitude
aswellasincreasedbeetleturnoveratlowlongitudesare inconsis‐
tent with t he expected ef fect of histor ic anthropogen ic pressure,
butmayalsobeexplainedbyamilderclimateinthewest.However,
wehavetopointoutthatwewerenotabletocollectF. fomentarius
samplesinthewesternmostregions(e.g.,England)duetotherarity
offruitbodiesofF. fomentarius.Moreover,manyofoursites,alsoin
western Europe,werelocatedinunmanagedforests(Figure1)and
althoug h forest manage ment had no eff ect on overall co mmunity
composition(SupportinginformationAppendixS3,FigureS3.2),the
gradientofanthropogenicpressuremaybelesspronouncedacross
oursitesthanatalandscapescale.
Environme ntal filtering by climatic dr ivers is often an imp ort‐
ant mecha nism struc turing commun ities (Cadot te & Tucker, 2017;
Kraftetal.,2015),includingdeadwood‐associatedinsectsandfungi
(Bässleretal.,2010;Mülleretal.,2012;Seiboldetal., 2016).Being
poikilothermic,arthropodsgenerally benefit fromhighertempera‐
tures (Sc howalter, 2006). However, we foun d a marginally sig nifi‐
cantnegativeeffectoftemperatureonalphadiversity.Onepossible
explana tion is that frui tbodies are dr ier and thus les s suitable for
somespeciesinwarmerclimates.However,ingeneralbetadiversity
wasnotaffectedbydissimilarityinclimaticconditions.Thissuggests
thatclimate is ofminorimportance for arthropodsassociatedwith
F. fomentarius despiteconsiderablevariabilityin climaticconditions
withinoursamplingrange(Figure1).
Theamountofavailablehabitatisoneofthefundamentaldriv‐
ers of biodiversit y (Fahrig, 2013; MacAr thur & Wilson, 1967). In
Europe, hu man activiti es over millennia have re duced the fores ts
and features of old‐growth stands (overmature and dead trees),
whichhasledtoadeclineofmanysaproxylicinsects(Seiboldetal.,
2015).Forestcover is only a coarse proxy for theamountofhab‐
itat available tospecies associated with dead wood or fruitbodies
ofF. fomentarius,astheamountof theiractualhabitat—dead wood
orfruitbodiesofF. fomentarius,respectively—canvaryconsiderably
within beech forests depending, for example, on current forest
management(Abregoetal.,2015;Bässler,Ernst,Cadotte,Heibl,&
Müller, 2014). This was als o reflected by t he time need ed to find
tenfruitbodiesofF. fomentarius inthepresentstudy,whichranged
fromminutestodays.Nevertheless,wefound thenumber of con‐
sumersamongfungicolousarthropodsandfungispecialistsamong
beetle s to increase with f orest cover (70 0m radius aroun d sites).
Consistentwithresultsofearlierstudiesthatfoundapositiveeffect
offruitbody availability on fungicolousbeetlediversity atregional
scales(Araujo,Komonen,&Lopes‐Andrade,2015;Rukke,2000),we
foundthenumberofarthropodspeciestoincrease withincreasing
fruitbodybiomass.Althoughourmeasureoffruitbodybiomassdid
notreflecttheabundanceofF. fomentarius atthesites,basedonour
resultscoveringarangeoffruitbodybiomassfrom0.4to21.7kgand
earlierfindingsatregionalscales(Araujoetal.,2015;Rukke,2000),
weexpectmorefungicolousarthropodspeciesinforestswithmore
fruitbodiesofF. fomentarius.
Forbeetles,samplesizestronglyaffectedthenumberofspecies
evenwhenaccountingforabundance,whichsuggeststhathabitat
heterogeneityincreaseswithfruitbodybiomass(Supportinginfor‐
mationAppendixS4,TableS4.1).Here,largersamplesseemtopro‐
videmoredifferenthabitatniches, forexample through different
stages of d ecomposition wi thin and among fr uitbodies (Dajoz et
al., 1966) similarl y as shown for coar se woody debri s (Seibold et
al.,2016).Concerningcommunitycomposition, only the totalbeta
diversity and turnovercomponent of predatory arthropods were
affected by sample size.However, abundance‐baseddissimilarity
in community composition ofb eetleswas affec ted by longitude
and sample size. Here, dissimilarity due to abundance gradients
(analogous to nestedness) increased with sample size. Overall,
this indic ates that loc al habitat amo unt is an impor tant driver of
alphadiversityoffungicolousarthropodcommunitiesand,atleast
for fungicolous beetle communities,an impor tant driver of beta
diversity.
BasedontheITSregion,Judovaetal.(2012)havesuggestedthat
populationsofF. fomentarius arecomprisedoftwosympatriccryptic
species;this hasbeen confirmedbyPristas, Gaperova,Gaper,and
Judova(2013)usingtheefagene.Onegenotype,termedgenotype
A, has b een suggested to b e prevalent on Europ ean beech whil e
the other,termed genotype B, isadditionally found on other host
species (Judova et al.,2012).Our geneticanalysisofF. fomentarius
supports this, as all but 5 of 36 of our samples—all sampledfrom
Europeanbeech—belongedtogenotypeA.Nevertheless,theoccur‐
renceofgenotype BonEuropeanbeechinthePyrenees,southern
Italy, Belgium andDenmark is a noteworthyresult(Supportingin‐
formationAppendixS1).Thelowintraspecificvariationamongsites
renderedananalysisoftheinhabitingarthropodcommunitybased
ongenetic differencesfruitless.Furtherstudiesareneeded to test
the hypothesis that F. fomentarius of genotype B hos ts arthro pod
communitiesdifferentfromgenotypeA.
Inour analyses, we incorporated variables whichare knownto
bestrongdriversoflarge‐scale differencesin communitycomposi‐
tion(Dobrovolski,Melo,Cassemiro,&Diniz‐Filho,2012;Soininen,
    
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 793
FRIESS E t al.
Lennon,&Hillebrand,2007;Zellweger,Roth,Bugmann,&Bollmann,
2017).Fur thermore,weaccountedfordifferencesinhabitatspe cial‐
ization andtrophic level,forestmanagementintensityand biogeo‐
graphicalregionsandevenconsideredthegeneticpropertiesofthe
fruitbodies.Nevertheless,whileourmodelsexplainedconsiderable
proportions ofvariationin alpha diversity most of the variation in
thecommunity compositionofarthropods occurringinfruitbodies
of F. fomentarius remained unexplained. Although explaining the
full variation in community composition was beyond the scope of
this study, these results appear surprising. We suggest three di‐
rections for future studies. First, future studies investigating the
community composition ofar thropods occurringin fruitbodies of
bracket fungishouldfocus on factors driving communitycomposi‐
tion at local scales.This mayincludethe amount of fruitbodies at
thesiteandlandscapescalewhichrepresenthabitatavailabilityand
mayaffectpopulationdynamicsviaincreaseddispersalsuccessand
rescueeffects givensufficientpatchconnectivity(Gonzalez,2005;
Snäll&Jonsson,2001;Venier&Fahrig,1996).Furthermore,studies
could inves tigate the ef fects of mic roclimate as me diated by can‐
opyopennessand forestsuccessional stage, whichwereshown to
generate largedifferencesincommunitycomposition in saproxylic
organisms (Hilmers etal., 2018;Seibold et al., 2016).Second, fur‐
therstudiesneedtoincludearthropodcommunitiesinfruitbodies
ofF. fomentariusonotherhost treespecies, suchas Betula spp. or
Populus spp.,andinvestigatepotentialalternativepost‐glacialrecol‐
onizationroutes.Third,to betterunderstand scale‐dependency of
communityturnover,futurestudiescouldcoverthewholerangeof
F. fomentariusincluding NorthAmericaandEast Asia.Forinstance,
theTenebrionidaeBolitophagus reticulatus isaubiquitousspeciesin
F. fomentarius fromEurope to Korea(Jung,Kim,&Kim, 2007), but
iscompletelyreplacedby itsrelative Bolitotherus cornutus inNorth
America(Matthewman &Pielou,1971),indicating thatthere might
beastrongerbiogeographicalstructuringofthecommunityatsuch
largerscales.
OurresultsshowedthatfruitbodiesofasinglefungusF. fomen‐
tarius pro vide habi t attoahi ghn u mberofar t h ropo d s,th e rebycon ‐
tributingconsiderablytobiodiversityinEuropeanbeechforests.
Conside ring the respon sibility of Europ ean countries t o protect
biodiversityinthisecosystem,werecommendmakingthepromo‐
tion of bra cket fungi as F. fomentarius an inte grated goal of for‐
estconservationstrategiesinEuropeanbeechforests.Theweak
biogeographicalstructuringandhighturnoverofcommunitiesbe‐
tweensites suggestthataprioritizationofcertainregionswithin
Europeisofminorimportancewithregardtoarthropodcommu‐
nitiesinF. fomentarius. Instead,werecommendthatconservation
should rangefromtheprotectionofforestswhere F. fomentarius
ishighlyabundantand inhabitedbyEurope‐widerarearthropod
species(e.g.,intheCarpathianMountains),totheretentionofin‐
dividualhabitattreesanddeadwoodwithfruitbodiesofthespe‐
ciesfromharvestingandsalvagelogging(includingunintentional
destructionbyloggingmachinery)throughoutEurope,andtothe
reintroductionof thespecies to regions(e.g., in westernEurope)
whereithasbecomeextinctandrelictpopulationsarelacking(for
methodssee Abrego etal., 2016).The example of the region of
Flanders,Belgium,showsthat F. fomentarius isabletorecolonize
areaswhereitwasformerlyextinctfromafewrelictpopulations
ifbee chd eadwoo dan dha bita ttr eesare ret aine d(Vande ke r khove
etal.,2011).Furthermore,manyfungicolousarthropodsareable
totrack F. fomentarius populationsrecolonizingsuitablehabitats
due to their high dispe rsal ability ( Vandekerk hove et al., 2011;
Zytynska et al.,2018). In addition topositiveeffects onspecies
associated with its fruitbodies, promoting F. fomentarius will po‐
tentially help to restore fundamental ecosys tem processes and
natural forest dynamicsinbeechforests as itisthe primaryde‐
composerofbeech woodand an importantagent of treesenes‐
cence and de ath. Species a ssociated with b roadleaf dead wo od
andsunnycondi tio nsi nfores t smaya lso benefitfro mga pscreated
when beech trees are killed byF. fomentarius. As F. fomentarius
provideshabitat,shapesfurtherhabitatcharacteristicsanddrives
ecosys tem processes, it c an be considered a key stone modifie r
orecosystemengineerinEuropeanbeechforests(Mills,Soule,&
Doak,1993).
ACKNOWLEDGEMENTS
Wearegratefultoallthosewhohelpe dinthef iel da ndinthelabo‐
rator y to conduct the s tudy, Svitlana Los for p roviding sampl es
fromCrimea,BorisBücheforidentificationofbeetlesandJérôme
Morinière for laboratory support in DNA barcoding. We thank
Emily Kilham for linguistic revision of the manuscript. Nicolas
Friessreceivedascholarship fromthe RudolfandHeleneGlaser
Foundation organized in the “Stifter verband für die deutsche
Wissenschaf t.”M.MikolášandM.Svobodaweresupportedbythe
Czech Universityof LifeSciences, Prague (CIGANo. 20184304)
andbythe institutional project MSMT CZ.02.1.01/0.0/0.0/16_0
19/0000803.
ORCID
Nicolas Friess https://orcid.org/0000‐0003‐0517‐3798
Jörg C. Müller https://orcid.org/0000‐0002‐1409‐1586
Simon Thorn https://orcid.org/0000‐0002‐3062‐3060
Sebastian Seibold https://orcid.org/0000‐0002‐7968‐4489
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BIOSKETCHES
Nicolas Friessresearchfocusesonlocal‐tolarge‐scalepat‐
ternsofbiodiversityinterrestrialecosystemsandtheassociated
processes.
Jörg C. Müller's re search focuses on forest biodiversity, from
ecological mechanisms toconservation strategies intemperate
forests,withaspecialfocusondeadwood‐relatedorganisms.
Sebastian Seibold's research focuses on the conservation of
biodiversity in forest ecosystems, particularly associated with
dead wood , and the impor tance of biodi versity for eco system
functioning.
SUPPORTING INFORMATION
Additional supporting information may be found online in the
SupportingInformationsectionattheendofthearticle.
How to cite this article:FriessN,MüllerJC,AramendiP,etal.
Arthropodcommunitiesinfungalfruitbodiesareweakly
structuredbyclimateandbiogeographyacrossEuropean
beechforests.Divers Distrib. 2019;25:783–796. ht tps://d o i .
org /10.1111/ddi.12882
Available via license: CC BY 4.0
Content may be subject to copyright.
... At large spatial scales, climatic conditions affect taxonomic alphaand beta-diversity as well as functional diversity of saproxylic communities (Baselga, 2008;Friess et al., 2019;Hagge et al., 2019). At smaller spatial scales, saproxylic communities can be strongly influenced by management-related changes in, for example, canopy cover, tree species composition and deadwood amount (Hagge et al., 2019;Seibold, Bässler, et al., 2015). ...
... At the European level including temperate and boreal countries, climatic variables explained beta-diversity of longhorn beetles (Cerambycidae) partly (Baselga, 2008), whereas no significant effects could be found for beta-diversity of saproxylic beetles inhabiting fruitbodies of the fungus Fomes fomentarius across temperate European beech forests (Friess et al., 2019). Our results suggest that climatic differences between plots were of minor importance for beta-diversity of saproxylic beetles since significant effects were found only in some years. ...
Drivers of community assembly change during succession in wood‐decomposing beetle communities
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  • Nov 2022
The patterns of successional change of decomposer communities is unique in that resource availability predictably decreases as decomposition proceeds. Saproxylic (i.e. deadwood‐dependent) beetles are a highly diverse and functionally important decomposer group, and their community composition is affected by both deadwood characteristics and other environmental factors. Understanding how communities change with faunal succession through the decomposition process is important as this process influences terrestrial carbon dynamics. Here, we evaluate how beta‐diversity of saproxylic beetle communities change with succession, as well as the effects of different major drivers of beta‐diversity, such as deadwood tree species, spatial distance between locations, climate and forest structure. We studied spatial beta‐diversity (i.e. dissimilarity of species composition between deadwood logs in the same year) of saproxylic beetle communities over 8 years of wood decomposition. Our study included 379 experimental deadwood logs comprising 13 different tree species in 30 forest stands in Germany. We hypothesized that the effects of tree species dissimilarity, measured by phylogenetic distance, and climate on beta‐diversity decrease over time, while the effects of spatial distance between logs and forest structure increase. Observed beta‐diversity of saproxylic beetle communities increased over time, whereas standardized effects sizes (SES; based on null models) of beta‐diversity decreased indicating higher beta‐diversity than expected during early years. Beta‐diversity increased with increasing phylogenetic distance between tree species and spatial distance among regions, and to a lesser extent with spatial distance within regions and differences in climate and forest structure. Whereas effects of space, climate and forest structure were constant over time, the effect of phylogenetic distance decreased. Our results show that the strength of the different drivers of saproxylic beetle community beta‐diversity changes along deadwood succession. Beta‐diversity of early decay communities was strongly associated with differences among tree species. Although this effect decreased over time, beta‐diversity remained high throughout succession. Possible explanations for this pattern include differences in decomposition rates and fungal communities between logs or the priority effect of early successional communities. Our results suggest that saproxylic beetle diversity can be enhanced by promoting forests with diverse tree communities and structures.
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... [37,38]), but usually within one taxonomic group or trophic guild at a time. The studies that have considered all arthropods are either exploratory, i.e. not inferring community patterns based on host traits [17,26,36], or limited to one or two fungal hosts [25,35,39]. However, to get a solid understanding of the effects of host traits in the fungi-arthropod system, we need to assess arthropod communities across different hosts. ...
... The most common families we identified consist mostly (Bolitophilidae, Mycetophilidae and Oppidae) or partly (Chironomidae and Cecidomyiidae) of fungivorous species [27,79,80]. However, fungivores may not necessarily be dominant, as our annotations are largely unresolved at the species level and predators could make up to a third of the faunal composition in fruit bodies [25,39]. At the order level, true flies and oribatid mites were dominant, which we expected based on earlier rearingbased studies on living fruit bodies of wood-decay fungi [17,26,27,34]. ...
DNA metabarcoding reveals host-specific communities of arthropods residing in fungal fruit bodies
Article
Full-text available
  • Feb 2022
Biological communities within living organisms are structured by their host's traits. How host traits affect biodiversity and community composition is poorly explored for some associations, such as arthropods within fungal fruit bodies. Using DNA metabarcoding, we characterized the arthropod communities in living fruit bodies of 11 wood-decay fungi from boreal forests and investigated how they were affected by different fungal traits. Arthropod diversity was higher in fruit bodies with a larger surface area-to-volume ratio, suggesting that colonization is crucial to maintain arthropod populations. Diversity was not higher in long-lived fruit bodies, most likely because these fungi invest in physical or chemical defences against arthropods. Arthropod community composition was structured by all measured host traits, namely fruit body size, thickness, surface area, morphology and toughness. Notably, we identified a community gradient where soft and short-lived fruit bodies harboured more true flies, while tougher and long-lived fruit bodies had more oribatid mites and beetles, which might reflect different development times of the arthropods. Ultimately, close to 75% of the arthropods were specific to one or two fungal hosts. Besides revealing surprisingly diverse and host-specific arthropod communities within fungal fruit bodies, our study provided insight into how host traits structure communities.
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... The very high diversity of TreMs across the range of both Fagus species implies a very high diversity of TreM-dwelling taxa. TreMs have been estimated to provide habitat for several thousand species, exemplified by the ~600 arthropod species present in the sporophores of tinder fungus (Fomes fomentarius) (Friess et al., 2019) and the ~380 species of beetles found in base rot-holes (Gouix and Brustel, 2012). ...
Drivers of tree-related microhabitat profiles in European and Oriental beech forests
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Tree-related microhabitats (TreMs) provide a quantitative indicator of habitat heterogeneity in forests, including beech (Fagus) forests. However, systematic analyses of the factors driving TreM diversity and composition in Fagus sylvatica and F. orientalis forests are lacking. In this study, the TreMs of beech forests on 203 plots of 22 forest sites (production and old-growth forest) across the full longitudinal range of both species were assessed following a standardized TreM protocol. A unified diversity and ordination framework based on Hill numbers was applied to account for unobserved TreM types and to extend the sensitivity of our findings focusing from rare to dominant TreMs. The composition of TreM assemblages was mostly determined by Fagus species and elevation, a surrogate for climate, and with focus on dominant TreMs by DBH, whereas old-growth versus production forest had no effect. The coverage of detected TreMs per plot increased with the number of trees assessed and DBH, but was lower in old-growth than in production forests. When standardized for sampling * Corresponding author at: Field Station Fabrikschleichach, 2 coverage, the diversity of rare and dominant TreM types was higher in old-growth than in production forests, but increased with elevation only focusing on dominant TreMs. These findings corroborate regional studies showing a higher TreM diversity in old-growth forests. Moreover, they demonstrate the importance of focusing conservation efforts on forests of both Fagus species and at different elevations, covering the full range of TreM assemblages. Future studies comparing TreM diversity in different forests should standardize diversity by sample coverage, as currently done in many biodiversity studies.
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... arthropods bats birds bryophytes fungi lichens molluscs trees vascular plants Ammer and Schubert (1999) x Bae et al. (2018) x Bardat and Aubert (2007) x Begehold (2017) x Blaser et al. (2013) x Boch et al. (2013a) x Boch et al. (2013b) x Bouget (2005) x Bouget et al. (2013) x Bouget et al. (2011) x Bouget et al. (2014) x Bouvet et al. (2016) x x Brin et al. (2011) x Burrascano et al. (2008) x Burrascano et al. (2017) x Charbonnier et al. (2016a) x Charbonnier et al. (2016b) x x Chumak et al. (2015) x Czeszczewik et al. (2014) x De Groot et al. (2016) x Díaz (2006) x Di Giovanni et al. (2015) x x Dormann et al. (2020) x Erdmann et al. (2006) x Friedel et al. (2006) x x Friess et al. (2019) x Grevé et al. (2018) x Gunnarsson et al. (2004) x Hanzelka and Reif (2016) x Hauck et al. (2013) x Heidrich et al. (2020) x x x x x x Heinrichs and Schmidt (2013) x Hofmeister et al. (2015) x x x Hohlfeld (1997) x Horak et al. (2014) x x x Humphrey et al. (2002) x x Ingle et al. (2020) x Jukes et al. (2002) x Kaufmann et al. (2018) x x x Király et al. (2013) x x Krah et al. (2018) x Kubartová et al. (2009) x Kubiak et al. (2016) x Kusch and Schotte (2007) x Laiolo (2002) x Laiolo et al. (2004) x Lange et al. (2014) x Leidinger et al. (2020) x x Loch (2002) x Machar et al. (2019) x Mag and Ó dor (2015) x Magura et al. (2000) x Márialigeti et al. (2009) x Márialigeti et al. (2016) x Mazziotta et al. (2016) x x x x x x x x Müller (2005) x x Müller et al. (2007) x Müller et al. (2008) x Müller et al. (2015) x Müller et al. (2018) x Nascimbene et al. (2013) x Nordén et al. (2003) x Ó dor et al. (2014) x x Paltto et al. (2008) x x Penone et al. (2019) x x x x x Petritan et al. (2012) x Poulsen (2002) x Preikša et al. (2016) x x x Przepióra et al. (2020) x Rosenvald et al. (2011) x Sabatini et al. (2014) x Schauer et al. (2018) x (continued on next page) approach have, to date, largely failed. ...
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... Logs and snags offer not only a larger amount of resources and higher niche diversity, which positively affect saproxylic diversity (Seibold et al., 2016b), but also a larger object surface. Thus, these stands favor the development of fungal species with larger fruiting bodies over time (Bässler et al., 2014), a food source for many saproxylics in beech forests (Friess et al., 2019). ...
Logging operations creating snags, logs, and stumps under open and closed canopies promote stand-scale beetle diversity
Article
Conservation tools to enrich habitat diversity in the widely distributed homogeneous production forests include stumps as logging residues but also the intentional creation of logs or snags, as well as varying canopy conditions. While an open canopy has been shown to foster forest biodiversity, the impact of different deadwood types at stand scale is less clear, which is crucial since this is the most relevant scale for silvicultural decisions. In this study, we experimentally manipulated canopy conditions (open vs. closed) and created deadwood (stumps, logs, snags) in different combinations in five mature European beech (Fagus sylvatica L.) forests to test the potential of active manipulations to increase the diversity of beetles, one of the most diverse insect orders in temperate forests. We estimated abundance, species number and species richness (controlled for abundance) of saproxylic (i.e., deadwood-dependent) and non-saproxylic beetles using flight-interception traps and analyzed species assemblages within the first 3 years of the experiment. Using generalized linear mixed effect models we found a 33.7 % and 43.4 % higher abundance as well as a 26.1 % and 23.5 % higher species number under open canopies for saproxylic and non-saproxylic beetles respectively, accompanied by a higher species richness of both groups. Stands with deadwood had a 38.6 % and 32.7 % higher species number followed by higher species richness of saproxylic and non-saproxylic beetles compared to stands without manipulation but manipulations did not affect beetle abundances. We identified sampling year, followed by canopy condition and deadwood type (in addition to an overall higher impact of spatial distance between stands and sites) by applying multiple regression analyses as most important to explain species assemblages of both beetle groups. Saproxylic abundance and species number in stump treatments were initially high but decreased over 3 years, while treatments containing snags and logs resulted in an increase in both abundance and species number over time. These temporal trends were mediated by canopy cover. Our findings provide three major insights for biodiversity-orientated management in mature beech forests: First, opening the canopy increases the stand-scale abundance, species number, and species richness of saproxylic and non-saproxylic beetles. Second, while stumps are attractive for saproxylics shortly after the logging operation, snags and logs provide longer-lasting deadwood resources, thus underlining longer sustainability of snag and log enrichment for forest biodiversity. Third, deadwood enrichment at the stand scale promotes not only deadwood-dependent but also other beetle species.
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... In protected beech stands, the most common woodboring fungus is Fomes fomentarius 82 . The most abundant microhabitats in our study were wood-decay fungi, especially of the genus Fomes, which are very important microhabitats for saproxylic beetles 83 . ...
Small-scale spontaneous dynamics in temperate beech stands as an importance driver for beetle species richness
Article
Full-text available
  • Jul 2022
Natural dynamics in forests play an important role in the lives of many species. In the landscape of managed forests, natural disturbances are reduced by management activities. This usually has a significant effect on insect diversity. The effect of small-scale natural dynamics of protected beech stands on the richness of saproxylic and non-saproxylic beetles was investigated. Sampling was carried out by using flight interception traps in the framework of comparing different developmental stages: optimum, disintegration, and growing up, each utilizing 10 samples. We recorded 290 species in total, of which 61% were saproxylic. The results showed that the highest species richness and thus abundance was in the disintegration stage. In each developmental stage, species variation was explained differently depending on the variable. Deadwood, microhabitats, and canopy openness were the main attributes in the later stages of development for saproxylic beetles. For non-saproxylics, variability was mostly explained by plant cover and canopy openness. Small-scale disturbances, undiminished by management activities, are an important element for biodiversity. They create more structurally diverse stands with a high supply of feeding and living habitats. In forestry practice, these conclusions can be imitated to the creation of small-scale silvicultural systems with active creation or retention of high stumps or lying logs.
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... So far, there have been rather few studies on the relationships between a whole set of TreMs and the abundance and diversity of forest-dwelling species. For example, birds' and bats' species richness was positively related to TreM diversity , while invertebrates showed positive associations with specific TreMs, like fruiting bodies of fungi or cavities (Friess et al., 2019;. Therefore, a better understanding of the links between a comprehensive set of TreMs and forest dwelling taxa may help to identify valuable habitat trees and provide a foundation for monitoring of some aspects of forest biodiversity. ...
The influence of retention forestry on the occurrence and abundance of forest birds across the landscape
Thesis
Full-text available
  • Jan 2020
Forests are undergoing through a slow but steady process of forest area change, which happen to be different across countries. Predictions of future scenarios highlight the role of agriculture in shaping land-use change in Europe, with possible local benefits for forests. Thus, the role of management in shaping the forests of the future will increase according to the World’s demand for timber, clean water, biodiversity, clean air and other ecosystem services. Research is testing and developing new management strategies to halt completely biodiversity loss. The threats faced by biodiversity in managed forests constitute the challenges of future forest ecological research. The response of birds to environmental changes is a consequence of the close-knit species-habitat relationships they evolved and are adapted to. Adaptations to the forest environment are structural, behavioural and physiological. The alteration of the forest structures and their spatial allocation across landscapes creates threats to bird populations that need to be taken into account in conservation-oriented forest management. The present thesis aims to assess the numerical response of the bird assemblage to forest structures and its relevance for management. The general aim is focused on close-to-nature forest management and on the retention of structural elements as a conservation tool. The numerical response of the bird assemblage is investigated in terms of species diversity and abundance. The general aim is achieved by focusing on the following research questions: i. Which forest and landscape characteristics best explain the abundance and diversity of forest birds? ii. Which management practices can be developed for the conservation of birds in managed forests? This thesis is carried out within the framework of the ConFoBi Research Training Group (Conservation of Forest Biodiversity in multiple-use landscape of Central Europe). ConFoBi assesses whether and how structural retention measures contribute to the conservation of forest biodiversity in multiple-use landscapes of the temperate zone. The research programme of the present thesis has been implemented in the southern Black Forest, Germany, as a model system for temperate forests. The Black Forest is a forest-dominated low mountain range within a multiple-use landscape typical of central Europe, where 135 quadratic 1-ha-plots where selected within the forested areas. Plots were selected along two major environmental gradients: forest vertical complexity, represented by the number of standing dead trees found in each plot; landscape composition, represented by the amount of forest cover within 25 km2 surrounding each plot. All plots were inventoried by measuring the diameter of every tree (above 7 cm diameter at breast height) and the amounts of laying and standing dead wood. Because habitat trees are an important structural element in retention approaches, for each study plot the 15 largest trees were mapped and their existing microhabitats (such as hollows, cracks, and cavities) quantified. Landscape patterns were described using a range of metrics, including amount of forest cover and landscape metrics. Bird data were collected by employing point counts performed at the centre of each plots and repeated two or three times per sampling season (2017-2018). Abundance and diversity of birds were analysed using hierarchical N-mixture models and generalized linear (mixed) models, respectively. The results highlight that current retention practices are well below the retention levels needed by the bird assemblage to have abundance and diversity similar to those of unharvested forests, assessing the levels around 40-60% of retained trees. Retention practices can, however, be improved by retaining trees of higher ecological importance. Trees with a diameter 20 cm larger than the surrounding trees, with cavities, rot holes or concavities can potentially fulfill the habitat requirments of a large array of species, including woodpeckers and the related cavity-users community. The presence of those trees across the landscape can ensure the continuity of resources, while favouring more natural tree species composition will benefit bird species diversity. The response of the entire bird assemblage to the configuration of forest patches indicates that in landscapes with less aggregated forest patches, the abundance of the bird assemblage can potentially be lower than in landscapes with closer forest patches. I conclude that the establishment and assemble of the bird community is a hierarchical spatial process. Small environmental elements determine the occurrence and observed abundance of populations. The location of such elements determines which species and how many individuals of each species are found across the landscape. Over the entire landscape, the amount of available habitat and its configuration determines how many species can be found at a given site. Therefore, I suggest a hierarchical set of actions should be considered, each benefiting birds at different levels of biological organization and spatial scale. Actions to preserve forest area and avoid fast land-use changes should have higher priority. The provisioning of large trees and deadwood would then ensure that the forests retain those structures and functions that support the establishment of bird populations in optimal habitats.
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... For example, the presence of perennial fungal fruiting bodies on European beech (Fagus sylvatica) very likely refers to the tinder fungus (Fomes fomentarius). The fruiting bodies of the tinder fungus was found to serve as habitat for up to 600 different arthropod species (Friess et al., 2019). Whereas the presence of perennial fungal fruiting bodies on silver fir (Abies alba) may refer to Phellinus hartigii, which presumably interacts with different arthropods compared to the tinder fungus (cf. ...
Occurrence and Development of Microhabitats at the single Tree and Forest Stand Level.
Thesis
  • Jan 2021
Habitat trees – one of the key elements of integrative retention approaches in European forests – are increasingly studied regarding their benefits to forest biodiversity. In this regard, treerelated microhabitats (TreMs) and deadwood serve as indicators of forest biodiversity. Specific recommendations of amounts of deadwood to be retained in managed forest stands to support related taxa are available, but not for TreMs. Retention of habitat trees aims to increase availability of TreMs in managed forests. To be able to refine selection criteria for habitat trees, I focused in this thesis on factors affecting TreMs on living trees. Therefore, I calculated species specific diameter thresholds bases on TreM occurrences, I investigated the effect of tree maintenance on TreMs in urban areas and I evaluated the short-term value of the retention of habitat tree groups. Chapter 1. The aim of this chapter was to explain TreM occurrence from a qualitative perspective by considering their diversity. Tree diameter at breast height (dbh), tree species, and canopy class were useful predictors of TreM diversity. TreM diversity on broad-leaved trees was on average higher than in conifers of the same diameter. In contrast to TreM abundance their diversity saturated towards higher dbh levels. Those TreM saturation levels were used to derive diameter thresholds. Habitat trees support not only more, but also more diverse, microhabitats in comparison to crop trees. Chapter 2. In this chapter I further developed the findings of chapter one and focused on the calculation of species specific diameter thresholds to precise recommendations for selecting habitat trees. Based on the relation between TreMs and tree diameter as well as TreMs and species I derived diameter thresholds for 18 European tree species (13 broad-leaved, 5 coniferous). Those thresholds refer to statistically disproportionate high levels of TreM richness or abundance. Complementing other aspects that need to be considered during habitat tree selection processes in managed forest stands, I recommend to select habitat trees with or close to a dbh of 70 cm for broadleaves and 86 cm for conifers. The differences of dbh thresholds between broadleaves and conifers as well as between species indicate species specific TreM dynamic. Chapter 3. In the third chapter, I investigated the TreM availability on urban trees along a maintenance gradient in Montréal, Canada. Intensive tree maintenance in urban trees led to levels of certain microhabitats such as cavities and injuries that were comparable to natural, unmanaged forests. Light maintenance of urban trees encouraged more crown deadwood than typical and intensive maintenance levels. My results underline the importance of conserving and maintaining large living trees, especially in urban areas to provide tree microhabitats. These results also demonstrate the important role of intensive tree maintenance in stimulating tree microhabitat development in urban areas. Chapter 4. Here, I addressed the effectiveness of habitat tree group (HTG) retention in forests of Baden-Württemberg, Germany, 10 years after the introduction of the approach. Large living trees (LLTs), standing deadwood and TreMs were significantly more abundant in HTGs than in reference plots. When retaining 5 % of a forest stand area as HTG, old-growth attributes increased significantly at the stand scale: amount of LLTs doubled and its volume almost tripled, and standing deadwood increased on average by 25 %. However, quantities of both attributes remain below recommended minimum thresholds. Retaining 5 % of stand area in HTG had a significantly positive effect on woodpecker cavities, rot holes and exposed heartwood, whereas 15 to 25 % area in HTGs would be required to increase stand level abundance of concavities, exposed sapwood or crown deadwood significantly. Retention of HTGs enriched managed, multiple-use forests with old growth structural attributes. Yet, the selection of HTGs could be made more efficient by focusing on forest patches with high tree volume or low tree density and by further considering snags, tree species mixture and LLTs as well as less vital trees. Overall the findings of this thesis suggest, that common tree attributes (species, diameter, vitality, canopy class, life status) can be used to predict the occurrence of TreMs. Species specific diameter thresholds can help to identify trees with higher levels of TreM richness. The specification of tree attributes in regard to TreMs allow to optimize habitat tree selection procedures. In addition or absence of trees rich in TreMs, tree maintenance could increase structural diversity. Intensively maintained trees providing comparable amounts of TreMs to trees from long-term unmanaged forests emphasize the relevance of artificially induced structures. To consider a holistic view on trees as biodiversity relevant feature throughout the landscape, I propose to expand further TreM research to urban and rural trees. Regardless how TreMs evolved and in which landscape they occur, the relation between TreMs and related taxa needs to be specified to strengthen the biodiversity indicating function of TreMs. Results from current TreM inventories, that followed standardized procedures, allow a approximation of TreM occurrence on a landscape level by linking species and diameter information to observed TreM abundances. To better understand development and persistence of TreMs repeated inventories were needed. Finally, my results allow to refine selection criteria of habitat trees based on the presence of TreMs and the consideration of species specific diameter thresholds. Furthermore, in absence of TreMs or when minimum diameters were not reached, I propose the possibility of artificial TreM creation to be useful for structural enrichment.
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Imprints of latitude, host taxon, and decay stage on fungus‐associated arthropod communities
Article
  • Mar 2022
Interactions among fungi and insects involve hundreds of thousands of species. While insect communities on plants have formed some of the classic model systems in ecology, fungus‐based communities and the forces structuring them remain poorly studied by comparison. We characterize the arthropod communities associated with fruiting bodies of eight mycorrhizal basidiomycete fungus species from three different orders along a 1200‐km latitudinal gradient in northern Europe. We hypothesized that—matching the pattern seen for most insect taxa on plants—we would observe a general decrease of fungal‐associated species with latitude. Against this backdrop, we expected local communities to be structured by host identity and phylogeny, with more closely related fungal species sharing more similar communities of associated organisms. As a more unique dimension added by the ephemeral nature of fungal fruiting bodies, we expected further imprints generated by successional change, with younger fruiting bodies harboring communities different from older ones. Using DNA metabarcoding to identify arthropod communities from fungal fruiting bodies, we find that latitude leaves a clear imprint on fungus‐associated arthropod community composition, with host phylogeny and decay stage of fruiting bodies leaving lesser but still‐detectable effects. The main latitudinal imprint is on a high arthropod species turnover, with no detectable pattern in overall species richness. Overall, these findings paint a new picture of the drivers of fungus‐associated arthropod communities, suggesting that latitude will not affect how many arthropod species inhabits a fruiting body, but rather what species occur in it and at what relative abundances (as measured by sequence read counts). These patterns upset simplistic predictions regarding latitudinal gradients in species richness and in the strength of biotic interactions.
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Sustainable management of naturally disturbed forests
Thesis
Full-text available
  • Jan 2021
Owing to climate change, natural forest disturbances and consecutive salvage logging are drastically increasing worldwide, consequently increasing the importance of understanding how these disturbances would affect biodiversity conservation and provision of ecosystem services. In chapter II, I used long-term water monitoring data and mid-term data on α-diversity of twelve species groups to quantify the effects of natural disturbances (windthrow and bark beetle) and salvage logging on concentrations of nitrate and dissolved organic carbon (DOC) in streamwater and α-diversity. I found that natural disturbances led to a temporal increase of nitrate concentrations in streamwater, but these concentrations remained within the health limits recommended by the World Health Organization for drinking water. Salvage logging did not exert any additional impact on nitrate and DOC concentrations, and hence did not affect streamwater quality. Thus, neither natural forest disturbances in watersheds nor associated salvage logging have a harmful effect on the quality of the streamwater used for drinking water. Natural disturbances increased the α-diversity in eight out of twelve species groups. Salvage logging additionally increased the α-diversity of five species groups related to open habitats, but decreased the biodiversity of three deadwood-dependent species groups. In chapter III, I investigated whether salvage logging following natural disturbances (wildfire and windthrow) altered the natural successional trajectories of bird communities. I compiled data on breeding bird assemblages from nine study areas in North America, Europe and Asia, over a period of 17 years and tested whether bird community dissimilarities changed over time for taxonomic, functional and phylogenetic diversity when rare, common and dominant species were weighted differently. I found that salvage logging led to significantly larger dissimilarities than expected by chance and that these dissimilarities persisted over time for rare, common and dominant species, evolutionary lineages, and for rare functional groups. Dissimilarities were highest for rare, followed by common and dominant species. In chapter IV, I investigated how β-diversity of 13 taxonomic groups would differ in intact, undisturbed forests, disturbed, unlogged forests and salvage-logged forests 11 years after a windthrow and salvage logging. The study suggests that both windthrow and salvage logging drive changes in between-treatment β-diversity, whereas windthrow alone seems to drive changes in within-treatment β-diversity. Over a decade after the windthrow at the studied site, the effect of subsequent salvage logging on within-treatment β-diversity was no longer detectable but the effect on between-treatment β-diversity persisted, with more prominent changes in saproxylic groups and rare species than in non-saproxylic groups or common and dominant species. Based on these results, I suggest that salvage logging needs to be carefully weighed against its long-lasting impact on communities of rare species. Also, setting aside patches of naturally disturbed areas is a valuable management alternative as these patches would enable post-disturbance succession of bird communities in unmanaged patches and would promote the conservation of deadwood-dependent species, without posing health risks to drinking water sources.
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Biodiversity along temperate forest succession
Article
Full-text available
  • Jul 2018
The successional dynamics of forests—from canopy openings to regeneration, maturation, and decay—influence the amount and heterogeneity of resources available for forest‐dwelling organisms. Conservation has largely focused only on selected stages of forest succession (e.g., late‐seral stages). However, to develop comprehensive conservation strategies and to understand the impact of forest management on biodiversity, a quantitative understanding of how different trophic groups vary over the course of succession is needed. We classified mixed mountain forests in Central Europe into nine successional stages using airborne Li DAR . We analysed α‐ and β‐diversity of six trophic groups encompassing approximately 3,000 species from three kingdoms. We quantified the effect of successional stage on the number of species with and without controlling for species abundances and tested whether the data fit the more‐individuals hypothesis or the habitat heterogeneity hypothesis. Furthermore, we analysed the similarity of assemblages along successional development. The abundance of producers, first‐order consumers, and saprotrophic species showed a U‐shaped response to forest succession. The number of species of producer and consumer groups generally followed this U‐shaped pattern. In contrast to our expectation, the number of saprotrophic species did not change along succession. When we controlled for the effect of abundance, the number of producer and saproxylic beetle species increased linearly with forest succession, whereas the U‐shaped response of the number of consumer species persisted. The analysis of assemblages indicated a large contribution of succession‐mediated β‐diversity to regional γ‐diversity. Synthesis and applications . Depending on the species group, our data supported both the more‐individuals hypothesis and the habitat heterogeneity hypothesis. Our results highlight the strong influence of forest succession on biodiversity and underline the importance of controlling for successional dynamics when assessing biodiversity change in response to external drivers such as climate change. The successional stages with highest diversity (early and late successional stages) are currently strongly underrepresented in the forests of Central Europe. We thus recommend that conservation strategies aim at a more balanced representation of all successional stages.
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vegan: Community Ecology Package. Ordination methods, diversity analysis and other functions for community and vegetation ecologists. Version 2.5-1. URL https://CRAN.R-project.org/package=vegan
Book
Full-text available
  • Apr 2018
The vegan package provides tools for descriptive community ecology. It has most basic functions of diversity analysis, community ordination and dissimilarity analysis. Most of its multivariate tools can be used for other data types as well. The functions in the vegan package contain tools for diversity analysis, ordination methods and tools for the analysis of dissimilarities. Together with the labdsv package, the vegan package provides most standard tools of descriptive community analysis. Package ade4 provides an alternative comprehensive package, and several other packages complement vegan and provide tools for deeper analysis in specific fields. Package https://CRAN.R-project.org/package=BiodiversityR provides a Graphical User Interface (GUI) for a large subset of vegan functionality. The vegan package is developed at GitHub (https://github.com/vegandevs/vegan/). GitHub provides up-to-date information and forums for bug reports. Most important changes in vegan documents can be read with news(package="vegan") and vignettes can be browsed with browseVignettes("vegan"). The vignettes include a vegan FAQ, discussion on design decisions, short introduction to ordination and discussion on diversity methods. A tutorial of the package at http://cc.oulu.fi/~jarioksa/opetus/metodi/vegantutor.pdf provides a more thorough introduction to the package. To see the preferable citation of the package, type citation("vegan").
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History and environment shape species pools and community diversity in European beech forests
Article
Full-text available
A central hypothesis of ecology states that regional diversity influences local diversity through species-pool effects. Species pools are supposedly shaped by large-scale factors and then filtered into ecological communities, but understanding these processes requires the analysis of large datasets across several regions. Here, we use a framework of community assembly at a continental scale to test the relative influence of historical and environmental drivers, in combination with regional or local species pools, on community species richness and community completeness. Using 42,173 vegetation plots sampled across European beech forests, we found that large-scale factors largely accounted for species pool sizes. At the regional scale, main predictors reflected historical contingencies related to post-glacial dispersal routes, whereas at the local scale, the influence of environmental filters was predominant. Proximity to Quaternary refugia and high precipitation were the main factors supporting community species richness, especially among beech forest specialist plants. Models for community completeness indicate the influence of large-scale factors, further suggesting community saturation as a result of dispersal limitation or biotic interactions. Our results empirically demonstrate how historical factors complement environmental gradients to provide a better understanding of biodiversity patterns across multiple regions.
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“Primeval forest relict beetles” of Central Europe: a set of 168 umbrella species for the protection of primeval forest remnants
Article
Full-text available
Identification of forest stands with priority for the conservation of biodiversity is of particular importance in landscapes with a long cultural and agricultural history, such as Central Europe. A group of species with a high indicator value for the naturalness of forest ecosystems are saproxylic insects. Some of these species, especially within the order Coleoptera, have been described as primeval forests relicts. Here, we compiled a list of 168 “primeval forest relict species” of saproxylic beetles based on expert knowledge. These species can serve as focal and umbrella species for forest conservation in Central Europe. They were selected because of their dependence on the continuous presence of primeval forest habitat features, such as over-mature trees, high amounts of dead wood, and dead wood diversity, as well as their absence in managed Central European forests. These primeval forest relict species showed a moderately strong clumping pattern within the phylogeny of beetles, as indicated by phylogenetic signal testing using the D-statistic. When we controlled for phylogenetic relatedness, an ordinal linear model revealed that large body size and preference for dead wood and trees of large diameter are the main characteristics of these species. This list of species can be used to identify forest stands of conservation value throughout Central Europe, to prioritize conservation and to raise public awareness for conservation issues related to primeval forests.