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ORIGINAL ARTICLE
Natural Disturbances are Essential
Determinants of Tree-Related
Microhabitat Availability
in Temperate Forests
Veronika Zemlerova
´,
1
Daniel Koza
´k,
1
* Martin Mikola
´s
ˇ,
1
Marek Svitok,
1,2
Radek Bac
ˇe,
1
Marie Smyc
ˇkova
´,
1
Arne Buechling,
1
Maxence Martin,
3
Laurent Larrieu,
4,5
Yoan Paillet,
6
Catalin-Constantin Roibu,
7
Ion Catalin Petritan,
8
Vojte
ˇch C
ˇada,
1
Matej Ferenc
ˇı
´k,
1
Michal Frankovic
ˇ,
1
Rhiannon Gloor,
1
Jen
ˇy
´k Hofmeister,
1
Pavel Janda,
1
Ondrej Kameniar,
1
Linda Majdanova
´,
1
Katka Markuljakova
´,
1
Radim Matula,
1
Marek Mejstr
ˇı
´k,
1
Milos
ˇRydval,
1
Ondr
ˇej Vostarek,
1
and Miroslav Svoboda
1
1
Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, Kamy
´cka
´129, 165 21 Praha 6 – Suchdol, Czech
Republic;
2
Department of Biology and General Ecology, Faculty of Ecology and Environmental Sciences, Technical University in
Zvolen, Masaryka 24, 960 01 Zvolen, Slovakia;
3
De
´partement des Sciences Fondamentales, Universite
´du Que
´bec a
`Chicoutimi, 555
boul. de l’Universite
´, Chicoutimi, Quebec G7H2B1, Canada;
4
Universite
´de Toulouse, INRAE, UMR DYNAFOR, Castanet-Tolosan,
France;
5
CNPF-CRPF Occitanie, Toulouse, France;
6
Univ. Grenoble Alpes, INRAE, UR Lessem, 2 rue de la Papeterie, BP76, 38402
Saint-Martin-d’Heres, France;
7
Forest Biometrics Laboratory–Faculty of Forestry, ‘Stefan Cel Mare’, University of Suceava, Univer-
sita
˘tii Street, No. 13, 720229 Suceava, Romania;
8
Department of Forest Engineering, Forest Management Planning and Terrestrial
Measurements, Faculty of Silviculture and Forest Engineering, Transilvania University of Bras¸ov, 500123 Bras¸ov, Romania
ABSTRACT
Assessing the impacts of natural disturbance on the
functioning of complex forest systems are impera-
tive in the context of global change. The unprece-
dented rate of contemporary species extirpations,
coupled with widely held expectations that future
disturbance intensity will increase with warming,
highlights a need to better understand how natural
processes structure habitat availability in forest
ecosystems. Standardised typologies of tree-related
microhabitats (TreMs) have been developed to
facilitate assessments of resource availability for
multiple taxa. However, natural disturbance effects
on TreM diversity have never been assessed. We
amassed a comprehensive dataset of TreM occur-
rences and a concomitant 300-year disturbance
history reconstruction that spanned large environ-
mental gradients in temperate primary forests. We
used nonlinear analyses to quantify relations be-
tween past disturbance parameters and contem-
porary patterns of TreM occurrence. Our results
reveal that natural forest dynamics, characterised
Received 16 August 2022; accepted 12 February 2023;
published online 27 March 2023
Supplementary Information: The online version contains supple-
mentary material available at https://doi.org/10.1007/s10021-023-0083
0-8.
Author Contributions: VZ, DK, MMik, MSvi, RB and MSvo conceived
the ideas and designed study; VZ, DK, MMik, ICP, CCR, VC
ˇ, PJ, OK,
MFer, MFra, RG, LM, KM, RM, MMej, MR and OV contributed to and
organised data collection; MSvi, VZ and MSmy analysed the data; VZ,
MMik, DK, AB, MM, LL, RG, YP, JHof, LM and ICP led the writing of the
manuscript. All authors contributed critically to the study and gave final
approval for publication.
*Corresponding author; e-mail: kozakd@fld.czu.cz
Ecosystems (2023) 26: 1260–1274
https://doi.org/10.1007/s10021-023-00830-8
Ó2023 The Author(s)
1260
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by fluctuating disturbance intervals and variable
severity levels, maintained structurally complex
landscapes rich in TreMs. Different microhabitat
types developed over time in response to divergent
disturbance histories. The relative abundance of
alternate TreMs was maximised by unique inter-
actions between past disturbance severity and
elapsed time. Despite an unequal distribution of
individual TreMs, total microhabitat diversity was
maintained at constant levels, suggesting that spa-
tially heterogeneous disturbances maintained a
shifting mosaic of habitat types over the region as a
whole. Our findings underscore the fundamental
role of natural processes in promoting conditions
that maximise biodiversity potential. Strict conser-
vation and management systems that preserve
natural disturbance outcomes, including associated
biological legacies, may therefore safeguard biodi-
versity at large scales.
Key words: TreM; disturbance history; primary
forests; dendroecology; biodiversity; carpathians.
HIGHLIGHTS
Natural disturbances generate TreMs, enhancing
habitat availability
TreM diversity did not change in time, alive vs.
dead trees show contrasting trends
Occurrence frequencies of TreM groups differ
with disturbance timings and severity
INTRODUCTION
Disturbances in Forest Ecosystems
Forest ecosystems that harbour a high proportion
of global terrestrial biodiversity are strongly influ-
enced by natural disturbances, local site conditions,
and climate (WCSFD 1999; Gustafsson and others
2012). Over the last decades, our understanding of
the environmental and short-term effects of natu-
ral disturbances has greatly improved (Sousa 1984;
Swanson and others 2010; Thorn and others 2017).
However, the long-term impact of natural distur-
bance history of varying frequency and severity in
shaping habitat structures for forest biodiversity has
rarely been assessed (Mori 2011; Yeboah and Chen
2016). The frequency, size and severity of distur-
bances are expected to increase with climate
change (Seidl and others 2014). The intensification
and potential interaction of future disturbance
processes highlights an essential need to better
understand the impacts of long-term natural dis-
turbance dynamics on habitat availability for forest
biodiversity.
TreMs, and Why to Study Their
Relationship with Disturbances
The biodiversity of several taxa cannot be easily
measured because taxonomic inventories are time
consuming and involve specialists; therefore, dif-
ferent indirect approaches and indicators have been
developed (Larsson and others 2001) such as ‘‘tree-
related microhabitats (TreMs) which are distinct,
well delineated structures occurring on living or
dead standing trees, that form a particular and
essential substrate or habitat for a great number of
species from various taxa’’ (Larrieu and others
2018). TreMs are gaining increasing attention in
forest management, conservation and research and
have been widely recognised as important biodi-
versity indicators in both protected and commercial
forests (Bu
¨tler and others 2004; Larrieu and others
2018). Although more evidence is needed to de-
scribe their relationships with species from many
taxonomic groups, in general, a positive correlation
between TreMs and local biodiversity has been
observed (Larrieu and others 2019; Asbeck and
others 2021b). TreMs are generally more abundant
and diverse in unmanaged than in managed forests
(Winter and Mo
¨ller 2008; Larrieu and others 2011;
Paillet and others 2017; Asbeck and others 2021a)
and the main drivers for the occurrence of TreMs at
the tree level are diameter (Paillet and others 2017;
Koza
´k and others 2018; Paillet and others 2019),
tree status (dead or alive) and tree species (Larrieu
and Cabanettes 2012; Koza
´k and others 2018;
Paillet and others 2019; Courbaud and others
2021). In primary forests, tree demography, diam-
eter distribution and mortality are driven by natu-
ral disturbance regimes; thus, they might have
profound effect on TreM density and diversity.
However, this relationship has not yet been well
documented (Martin and others 2021).
The Effect of Natural Disturbances
on TreMs
Natural disturbances play a key role in shaping the
structural heterogeneity of forest ecosystems and
habitat provisioning for biodiversity. Standing
deadwood and deadwood density formed by dis-
turbances are crucial for the presence of TreMs
(Donato and others 2012; Meigs and others 2017).
TreMs can be formed by a direct injury (bark loss)
Natural Disturbances are Essential Determinants 1261
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or injuries formed over longer time periods (decay
cavities), by both abiotic (fractures in the trunk,
fractures of branches, cracks caused by windstorms
or in rare cases by lightning strikes) and biotic
factors (insect galleries formed by bark–beetles)
(Larrieu and others 2018). These injuries can
immediately provide habitat opportunities for a
great number of species from various taxa (Larrieu
and others 2018;Bu
¨tler and others 2020). Other
TreM types, such as cavities, need more time for
development; rot-holes in particular require several
decades to several hundreds of years to form
(Bu
¨tler and others 2020). The presence of dead
trees facilitates the occurrence of cavities as well as
bark shelters, bark pockets or fungi. Moreover,
disturbances also affect forest structure. The time
since disturbance and severity of disturbance are
good predictors of DBH (diameter at breast height)
distribution (Janda and others 2017; Rodrigo and
others 2022). Considering the positive correlation
of TreM abundance with DBH (Koza
´k and others
2018; Paillet and others 2019), we hypothesise that
disturbance dynamics affect TreM diversity, and
that occurrence frequencies of individual TreM
groups would respond differently to disturbance
characteristics, as the forest provides different
conditions (DBH and age distribution, proportion of
snags and deadwood) after a disturbance event.
TreMs in Primary Forests
Primary forests, defined as a forest without direct
human impacts (Sabatini and others 2018; Mikola
´s
ˇ
and others 2019), are of outstanding biological and
cultural value (Watson and others 2018). They
provide optimal conditions for many endangered
and rare species, and they enable us to gain crucial
insight into the complex interrelationships be-
tween biodiversity and the evolutionary pressures
of natural disturbances (Sabatini and others 2018).
Recent studies show that primary forests host a
greater total richness of TreMs and abundance of
some specific types than their managed counter-
parts (Winter and Mo
¨ller 2008; Paillet and others
2017; Asbeck and others 2021a). Higher richness of
TreMs in primary forests may be explained by the
higher occurrence of large and old living trees with
crown deadwood and snags, as these habitat trees
bear large amounts of TreMs and do not occur in
such high numbers in managed forests. Further,
primary forests typically consist of heterogeneous
conditions as they have high variation in DBH and
tree age, which are the result of natural distur-
bances (Stokland and others 2012). As such, pri-
mary forests remain the only places that enable us
to gain crucial insight into the complex interrela-
tions between TreMs and long-term natural dis-
turbance histories. In contrast, in managed forest,
the constant removal of trees or parts of trees that
show ‘‘defects,’’ such as exposed sap- and heart-
wood or crown deadwood created by natural dis-
turbances, provides a hindrance to disentangling
the long-term natural disturbance effects on TreMs
(Martin and Raymond 2019).
The study settings allowed us to assess a full
range of diverse disturbance histories on TreMs
occurrence. Using a unique dendroecological dis-
turbance history reconstruction (Schurman and
others 2018) from European temperate primary
spruce forests across the Carpathian Mts., we
examine the relative importance of natural histor-
ical disturbance regimes in shaping TreMs occur-
rence and diversity. For the Carpathian Norway
spruce [Picea abies (L.) Karst.] forests, mixed-
severity disturbance regimes with high variability
of severities and frequencies have been identified
as the dominant driver of forest dynamics (Svoboda
and others 2014; Janda and others 2017; Trotsiuk
and others 2014; Schurman and others 2018). The
main disturbance agents in temperate Europe are
wind and bark–beetle (Ips typographus) outbreaks
(Temperli and others 2013;C
ˇada and others 2016;
Holeksa and others 2017). We addressed three
main research questions: (1) How does the distur-
bance severity and time since the most severe dis-
turbance on a plot level affect TreM diversity? (2)
In which development phase (early-seral, mid-
seral, late-seral) does TreM diversity reach its peak?
(3) Are there any differences in how disturbance
severity and time since the most severe disturbance
affect occurrence frequencies of individual TreM
groups?
MATERIAL AND METHODS
Study Sites
Our study was conducted in primary temperate
forests in the Slovak and Romanian part of the
Carpathian Mountains, which are amongst the
countries with the highest extent of primary forests
in continental Europe (Sabatini and others 2018;
Mikola
´s
ˇand others 2019). These forests developed
under natural disturbance dynamics and have not
been affected by human management over the last
century at least, mainly due to montane topogra-
phy and remote location (Sabatini and others
2018). Primary forests of the Carpathian Moun-
tains are dominated by Norway spruce [Picea abies
(L.) Karst.]. Admixed tree species, such as fir (Abies
1262 Veronika Zemlerova
´and others
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alba Mill.), rowan (Sorbus aucuparia L.), pine (Pinus
cembra), beech (Fagus sylvatica) and birch (Betula
spp.) were present only on some plots. The climate
of the Carpathians is broadly classified as cool-hu-
mid, with mean precipitation of 1100 mm and mid-
altitude (1000 m a.s.l.) annual temperatures of
4.5°C over the past half a century (Spinoni and
others 2015).
We conducted our research in 13 forest stands in
Slovakia and 13 stands in Romania (Table 1; Fig-
ure 1). We collected data from 297 permanent
circular research plots with an area of 1000 m
2
(17.84 m radius from the plot centre). The plots
were established in selected polygons of primary
forests using a stratified random design (Svoboda
and others 2014). All the plots are part of a long-
term research network studying natural forest
dynamics in primary forests (Remote Primary For-
est 2021). Within each plot, positions of all living
and dead trees >60 mm in diameter at breast
height (DBH) were recorded using a laser range-
finder with compass and customised software Field-
Map (Field-Map; Monitoring and Mapping Solu-
tions, Jı´love
´u Prahy, Czech Republic).
TreM Survey
We visually inspected every standing dead or live
tree on a plot with DBH greater than 60 mm for
TreM presence based on typology by Larrieu and
others (2018) which consists of 15 groups (for
example, woodpecker breeding cavities) and 45
types (Table 2). In further analysis, we worked only
on a group level to have sufficient statistical power.
In total, we inspected 22,108 trees and quantified
TreM diversity and abundance for each plot.
Diversity was defined as TreM richness, that is, the
number of TreM groups occurring in a plot.
Abundance was recorded for every TreM group
individually and was defined as a number of trees
on a plot bearing a given TreM group.
Table 1. Characteristics of the Study Area
Country Location Stand n
plots
Mean nof
trees per plot
TreMs Time since (years) Severity (% CA)
Mean
richness
Mean
abundance
Min Max Mean Min Max Mean
Romania Fagaras 1 12 85.2 7.9 106.2 42 227 120.2 21 74 41.3
2 12 89.1 8.3 169.9 47 227 147.7 23 94 48.8
3 12 86.1 9.2 171.8 52 200 142.3 22 72 48.3
4 12 88.2 9.3 159.2 4 236 141.1 19 76 34.9
5 12 66.2 7.8 121.3 98 215 152.1 35 100 53.0
6 13 93.8 8.2 118.6 36 187 124.3 20 91 40.0
7 12 58.7 8.7 105.0 1 191 147.0 17 49 36.7
8 11 74.4 7.7 105.0 6 120 90.3 23 80 49.8
9 12 91.3 8.2 151.8 81 141 103.3 27 73 48.0
10 12 75.8 8.3 157.3 104 252 148.6 22 92 55.3
Giumalau 11 11 97.1 8.6 128.2 39 258 153.7 23 60 38.6
12 22 91.5 8.0 91.1 2 315 113.0 22 83 48.2
13 13 81.7 8.8 142.0 2 202 131.3 24 97 56.4
Slovakia High Ta-
tras
14 5 89.2 8.8 133.0 3 170 69.6 17 97 62.6
15 9 60.9 9.0 113.8 3 84 13.2 29 98 68.4
16 8 74 10.0 178.8 3 196 66.4 24 100 58.1
17 7 83.1 7.6 101.3 3 151 83.4 19 96 36.9
18 7 65.4 9.1 173.3 7 194 111.6 23 85 42.4
19 14 60.2 7.6 93.6 2 217 101.1 21 98 40.1
20 10 96.5 8.8 109.2 8 139 67.8 31 62 49.4
Low Ta-
tras
21 10 55.2 9.5 64.5 3 149 75.4 24 72 37.5
22 15 61.1 8.5 86.8 3 195 140.5 21 67 40.5
Great Fa-
tra
23 25 43.9 8.6 55.8 3 269 123.9 18 92 41.0
24 5 34.6 9.8 69.0 1 147 59.2 32 93 66.2
Orava
Beskids
25 6 35 9.7 74.3 3 198 91.2 17 93 42.3
Polana 26 5 81.6 10.4 229.0 99 154 127.8 32 95 58.2
CA: canopy area removed by disturbance as a percent of the total canopy area of the stand.
Natural Disturbances are Essential Determinants 1263
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Disturbance Characteristics
Disturbance history was reconstructed using
increment cores collected from the permanent
study plot network. The derived chronologies pro-
vided data for approximately the last 250 years.
The increment cores were collected from 25 trees
selected randomly from the non-suppressed living
trees with DBH at least 10 cm in each plot, 1 m
above the ground and processed for laboratory
analysis. The tree-ring widths were measured with
the LintabTM sliding-stage measuring device
(Rinntech, Heidelberg) with a resolution of
0.01 mm. Cores were visually cross-dated and
verified using COFECHA (Holmes 1983). The
reconstruction of disturbance events was based on
the assumption that disturbance processes affect
levels of neighbourhood competition and resource
supply, and hence, growth responses in extant
individuals (Svoboda and others 2014). Statistically
anomalous tree growth variation exceeding site-
specific thresholds and sustained over minimum
pre-defined temporal intervals was attributed to
disturbance-driven gap formation events (Frelich
2002; Trotsiuk and others 2014). Severity of the
disturbance event was then defined in terms of the
proportional area of tree canopy removed. An
estimate of the canopy area removed was calcu-
lated using regression methods and allometric
equations relating the aggregate present-day size of
tree responders (individuals with a disturbance
signal) to the original extent of the disturbance-
induced canopy gap (Lorimer and Frelich 1989).
For each plot we, identified the main disturbance as
the event with the maximum severity (proportion
of canopy area disturbed). Number of years since
Figure 1. aMap of the research area indicating the location of the study sites. Stands are represented by green triangles.b
Inset map shows a study region within Europe represented by a black bounding box.cExample arrangement of plots within
one stand. dExample arrangement of trees within one plot.
1264 Veronika Zemlerova
´and others
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
the main disturbance was calculated by subtracting
the year of this event from the year of data col-
lection. For recently disturbed plots, where the
current canopy area disturbed was larger than
dendrochronologically detected maximum distur-
bance severities, the severity was expressed by
current canopy openness. Relative current canopy
openness was calculated as the difference between
mean canopy closure of the whole dataset and
current canopy closure of a given plot (Bac
ˇe and
others 2017). Time since these recent disturbances
was calculated based on the decay stage (Aakala
and others 2006) of the majority of standing dead
trees on a plot as an average estimated time since
death for individual stages as the year of the mea-
surement minus 1 year for trees with status 1 (re-
cently dead, there are small twigs with leaves),
3 years for trees with status 2 (recently dead, there
are small twigs without leaves) or 5 years for trees
with status 3 (small twigs not visible, but big
branches are present) (unpublished data, Bac
ˇe).
We defined disturbance events as ‘‘low severity’’
(characterised by events severity below 40%),
‘‘moderate severity’’ (between 40 and 60%) and
‘‘high severity’’ (affecting more than 60% of ca-
nopy trees) (Janda and others 2017). For detailed
disturbance characteristic descriptions and calcula-
tions, we refer readers to Appendix 1 and C
ˇada and
others (2020).
Data Analysis
Generalised additive mixed models (GAMMs,
Wood 2017) were used to test the effect of time
since maximum disturbance and severity on the
TreM profile (TreM diversity and TreM occurrence
frequencies of individual TreM groups) in the forest
plots. We treated stand identity as a random effect
in the models to account for the hierarchical design
of the study (that is, plots nested within stands).
The TreM diversity (number of TreM groups
occurring on a plot for total, alive and dead trees)
was used as a response variable in GAMM with
gaussian error distribution and logarithmic link
function. The occurrence of individual TreM groups
was modelled as binomial frequencies (proportion
of trees bearing a given group out of all trees
sampled in a plot) with a logit link function. Thin
plate regression splines were used as base smooth-
ers in the GAMMs (Wood 2003). We examined
diagnostic plots of residuals to check the perfor-
mance of the models. Because the dispersion
parameters of some binomial GAMMs deviated
from one, the standard errors of these models were
estimated by a quasi-likelihood procedure. The
analysis was performed in R v. 3.6.1 (R Core Team
2019) using the libraries DHARMa (Hartig 2022)
and mgcv (Wood 2017).
Table 2. TreM Typology Used in This Study Based on Larrieu and Others (2018)
TreM group Type
Woodpecker breeding cavities Small, medium, large woodpecker breeding cavities and woodpecker flute
Rot-holes Trunk base rot-hole, trunk rot-hole, semi-open trunk rot-hole, chimney trunk base
rot-hole, chimney trunk rot-hole and hollow branch
Insect galleries Insect galleries and bore holes
Concavities Dendrotelm, woodpecker foraging excavation, trunk bark-lined concavity and root-
buttress
Exposed sapwood only Bark loss, fire scars, bark shelter and bark pockets
Exposed sapwood and heartwood Stem breakage, limb breakage, crack, lightning scar and fork split at insertion
Remaining broken limb Remaining broken limb
Twig tangles Witch broom, epicormic shoots
Burrs and cankers Burr, canker
Perennial fungal fruiting bodies Perennial polypore
Ephemeral fungal fruiting bodies
and slime moulds
Annual polypore, pulpy agaric, large pyrenomycetes and myxomycetes
Epiphytic and parasitic crypto- and
phanerogams
Bryophytes, lichens, ivy and lianas, ferns, mistletoe
Nests Vertebrate and invertebrate nest
Microsoils Bark and crown microsoil
Exudates Sap run and heavy resinosis
Natural Disturbances are Essential Determinants 1265
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RESULTS
TreM Diversity
The diversity of TreM groups was significantly
influenced by time since the maximum disturbance
for both live and standing dead trees. Alive trees
showed contrasting trend compared to dead trees.
Whilst total TreM occurrence on living trees had a
U-shaped response to time since disturbance, being
highest early after a disturbance and then in late-
seral development phases, TreMs diversity on
standing dead trees increased after a disturbance
event and subsequently fluctuated in the mid
development phases. The total number of TreM
groups did not significantly change through (Ta-
ble 3; Figure 2). Recently disturbed plots showed
diversity comparable to those disturbed later than
150 years ago. We found a significant relationship
with disturbance severity and number of TreM
groups for live trees; diversity increased marginally
with severity. For total and dead trees, the rela-
tionship with severity was not significant (Table 3;
Figure 2).
Occurrence Frequencies of Individual
TreM Groups
Amongst the 15 investigated TreM groups, the
probability of the occurrence of ten groups was
significantly influenced by time since maximum
severity disturbance and/or severity of that event
(Table 3). The highest occurrence frequencies were
more or less evenly distributed in the disturbance
space (Figure 3). Only insect galleries and exposed
sapwood followed a similar pattern with severity,
reaching the highest occurrence frequencies in
strongly disturbed forest plots. For insect galleries,
time was also significant, and the highest occur-
rence frequencies was reached either in recently
disturbed plots, or plots disturbed around 250 years
ago. Ephemeral and perennial fungal fruiting bod-
ies followed a similar pattern with time; they had
higher occurrences in recently disturbed plots and
another peak 140 and 200 years ago, respectively.
The different fungal groups also differed in their
response to disturbance severity, with ephemeral
fungal fruiting bodies occurring most often at low
severities, whilst perennial fungal fruiting bodies
were more frequent at moderate severities. Nests
Table 3. Summary of GAMMs Testing for the Effect of Time Since Max. Disturbance and Severity of that
Event on TreM Groups Diversity and on Occurrence Frequency of TreM Groups in Forest Plots
Time since maximum
disturbance
Maximum disturbance
severity
Stand
Variable edf x2/Fp edf x2/Fp edf x2/Fp
TreM diversity
Total 1.00 1.693 0.194 1.00 2.361 0.126 19.51 3.020 <0.001
Alive 7.79 2.877 0.003 1.28 12.247 <0.001 18.72 2.487 <0.001
Dead 2.45 5.73 <0.001 2.03 0.78 0.401 19.63 3.40 <0.001
Occurrence frequencies
Woodpecker breeding cavities 1.00 0.416 0.5196 1.00 4.014 0.0461 20.66 7.117 <0.001
Rot-holes 1.00 2.515 0.114 1.86 2.192 0.140 19.86 5.174 <0.001
Insect galleries 4.50 8.718 <0.001 1.00 29.336 <0.001 19.90 4.108 <0.001
Concavities 2.32 3.530 0.021 1.00 1.457 0.228 12.04 1.112 <0.001
Exposed sapwood only 1.00 1.696 0.194 1.00 7.609 0.006 18.44 3.017 <0.001
Exposed sapwood and heartwood 1.00 0.719 0.397 1.56 1.069 0.337 15.30 1.883 <0.001
Remaining broken limb 1.00 2.025 0.156 1.00 0.600 0.439 19.48 1.815 <0.001
Twig tangles 1.00 3.737 0.054 1.00 1.620 0.204 16.73 0.942 0.107
Burrs and canker 1.00 0.727 0.394 1.00 14.260 <0.001 15.66 49.293 <0.001
Perennial fungal fruiting bodies 4.90 34.20 <0.001 2.49 10.87 0.014 20.72 127.19 <0.001
Ephemeral fungal fruiting bodies 3.81 2.501 0.038 1.00 4.814 0.029 18.43 5.217 <0.001
Epiphytic and parasitic crypto- and
phanerogams
3.09 4.569 0.001 1.00 3.745 0.054 20.69 5.582 <0.001
Nests 4.75 18.833 0.003 1.00 4.645 0.031 14.54 50.723 <0.001
Microsoils 2.05 2.678 0.092 1.00 0.091 0.764 20.33 4.903 <0.001
Exudates 5.45 3.698 0.001 1.00 14.286 <0.001 19.49 4.391 <0.001
The effective degrees of freedom (edf), test statistics (F/v
2
) and probabilities (p) are displayed. Results significant at a= 5% are highlighted in bold. Note that the stand identity
(n = 26) was treated as a random effect in the models.
1266 Veronika Zemlerova
´and others
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were typical for recent, low-severity disturbances
with another peak about 170–200 years ago. Exu-
dates also had the highest occurrence frequencies
with low severities and had two peaks representing
disturbances that occurred 50–60 years ago and
250–260 years ago. Concavities and epiphytic and
parasitic crypto- and phanerogams reached the
highest frequencies on plots disturbed about 100–
150 years ago. Finally, woodpecker breeding cavi-
ties and burrs and cankers occurred most fre-
quently on plots disturbed by low severities.
DISCUSSION
We conducted the first empirical study on the
relationship between present-day TreM profile
(frequencies and diversity) and natural disturbance
history of European spruce primary forests. Our
results show that natural forest dynamics charac-
terised by variable disturbance severities, their
timing and multiple successional pathways main-
tained forest landscapes rich and diverse in tree-
related microhabitats. Whilst total TreM groups
diversity was not significantly affected by distur-
bance history in the primary forests, the effect of
disturbance severity and timing differed signifi-
cantly amongst live and dead trees and particular
TreM groups.
Effect of Natural Disturbance on Total
Trem Diversity
Despite the contrasting trends of TreM diversity
between living trees, which followed similar trends
as found in previous studies from primary forests
(Martin and others 2021), and dead trees, the total
diversity of TreMs did not significantly change in
time, which is in accordance with results by Larrieu
and others (2014). As we analysed the total TreM
diversity at the plot level, the sharp increase in
diversity in the initial phase after a disturbance
amongst dead trees can be explained by an increase
in the number of dead trees, and conversely, the
decline of TreMs amongst live trees was caused by
the decline in the number of living trees. This
interesting pattern maintains balanced TreMs
diversity across different developmental phases in
the primary forests and shows that high biodiver-
sity potential and complexity may persist through
Figure 2. Result of GAMM showing relationships between the diversity of TreM groups, time since the most severe
disturbance and disturbance severity (% canopy area removed). Predicted diversity (line) is displayed along with 95%
confidence intervals (band). Significant relationships (p<0.05) are represented by solid lines and non-significant
relationships by dashed lines.
c
Figure 3. Predicted occurrence frequencies (isolines) of
ten TreM groups along the gradients of maximum
disturbance severity and time since that event.
Occurrence frequencies are predicted by significant
GAMMs. For model details see Table 3(miniatures of
TreMs are courtesy of Kraus and others 2016).
Natural Disturbances are Essential Determinants 1267
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
1268 Veronika Zemlerova
´and others
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
natural forest development after disturbances
(Donato and others 2012; Meigs and others 2017).
Disturbance severity had a significant effect on
TreM diversity for live trees, whilst there was no
significant pattern found for total and dead trees. This
observed pattern might be explained by the natural
disturbance regime of the studied primary forests.
The studied area (the Carpathian Mountains) is
characterised by a mixed-severity disturbance regime
with predominant low and moderate disturbance
severities (Janda and others 2017). The mean dis-
turbance severity in our dataset varies from 34.9 to
68.4% between stands and moderate severity dis-
turbance are the most frequent disturbance types.
Moderate severity disturbances leave behind com-
plex forest structures, including a significant number
of standing mature live and dead trees (C
ˇada and
others 2020) bearing high TreMs diversity. They also
cause injuries on remaining trees that could further
develop into TreMs. The highest TreM abundance
and diversity on the tree level are typically found on
snags and large trees (Paillet and others 2017;Koza
´k
and others 2018; Paillet and others 2019). Due to
prevalence of moderate severity disturbances in the
studied areas and the lack of stand-replacing distur-
bance events that cause mortality of almost all trees,
the diversity of TreMs did not significantly change
with disturbance severity. However, the effect of
natural disturbances on occurrence frequencies dif-
fers between individual TreM groups.
Effect of Natural Disturbance on TreM
Groups Occurrence Frequencies
To fully understand the effect of natural distur-
bance on TreM diversity and occurrence, it was
essential to show the individual responses of par-
ticular TreM groups, as each of them represents
essential habitats for different forest-dwelling
organisms. Here, not only the effect of disturbance
timing but also the effect of disturbance severity
played an important role.
Low Severity
(1) Burrs and cankers occurred on plots disturbed
with low severities. For the creation of these struc-
tures, the tree has to survive the disturbance, and
the occurrence rate increases with DBH (Courbaud
and others 2021). Comparably we observed the
highest occurrence frequencies on plots disturbed
with low severities for (2) woodpecker breeding
cavities. They are often present on snags or large
living trees. The key significance of tree suitability
for woodpeckers depends on DBH, tree age and
fungal decay that soften the wood (Newton 1994;
Jackson and Jackson 2004;Bu
¨tler and others 2004;
Basile and others 2020). Similarly, we observed co-
occurrence pattern with conks of fungi, which was
observed also by Larrieu and others (2022).
Low Severity and Two Peaks in Time
(3) Nests, which consist of vertebrate and inverte-
brate nests, occur in the highest frequencies in re-
cently disturbed plots with low severities, as they
can be destroyed by high severity events. The sec-
ond peak occurred about 170–200 years after the
disturbance event, which can be linked with the
presence of senescent, large trees. Similarly (4)
exudates occur in plots disturbed with low severi-
ties and can be formed by subsequent disturbances
with even lower severities, such as a single tree fall
that injures other trees that remain alive. (5)
Ephemeral fungal fruiting bodies and (4) perennial
fungal fruiting bodies were significantly related to
time and severity of disturbances. They follow a
similar pattern with time and are most frequent
right after a disturbance event, when trees can be
infected after bark injury caused by a disturbance;
thus, both groups profit from new substrate avail-
ability. The other peaks occur 140 and 200 years,
respectively, after the disturbance event, which
may be explained by mortality of senescent trees
that survived the disturbance. However, the groups
differ in relationship with severity. As a group of
ephemeral fungal fruiting bodies covers a wide
range of fungi groups with different ecological de-
mands (Pouska and others 2010; Holec and others
2020), the higher occurrence can therefore indicate
the higher heterogeneity of conditions caused by
low severity disturbances. On the other hand,
maximum occurrence of perennial fungal group
represented only by perennial polypores after
moderate severity disturbance (55–85%) can be a
response to more homogenous conditions created
by disturbance as the perennial polypores group is
in spruce stands dominated by Fomitopsis pinicola,
which is the common species in disturbed forests
and occurrence of its fruiting bodies decreases with
ongoing decay process (Pouska and others 2011,
Ba
¨ssler and others 2015; Holec and others 2020).
Time
(7) The group concavities consist mainly of root-
buttress concavities in our dataset; they are formed
on trees with roots large enough to bear such TreM
(Chiatante and others 2002; Courbaud and others
2021). The highest occurrence frequency was
found about 80–170 years after the most severe
disturbance. That can be explained by the fact that
Natural Disturbances are Essential Determinants 1269
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
they are not formed directly by disturbance, but
need the presence of large trees as they are more
abundant on trees with higher DBH (Asbeck and
others 2021b). (8) Epiphytic and parasitic crypto-
and phanerogams represented mainly lichens and
mosses whose frequencies were highest 100–
170 years after disturbance. According to (Tanona
and Czarnota 2022), the presence of natural forest
disturbances increases lichen diversity in Car-
pathian spruce forests. After a short-term period of
stabilisation following a disturbance event, the
diversity of lichens increases. Due to the slow
growth rate that is typical for lichens, they need
enough time to gain significant size. Bryophyte
diversity is mainly dependent on microclimatic
conditions, with epixylic bryophyte abundance
supported by a dense canopy closure (Raabe and
others 2010) therefore, the abundance may be
lower immediately after disturbance.
High Severity
(9) Insect galleries reached an occurrence fre-
quency maximum right after a disturbance event
with high severity; the second peak occurred after
250 years. The second peak around 250 years after
the most severe disturbance might be connected to
another less severe disturbance event that may
have affected the trees that survived the most
severe one. Their formation is relatively rapid and
require just several years to develop. Bark–beetle
outbreaks are one of the most important distur-
bance agents in Carpathian spruce forests (Temperli
and others 2013). As the development of insect
galleries is very quick (Bu
¨tler and others 2020),
these injuries can further develop in other TreMs.
(10) Exposed sapwood followed a similar pattern;
however, we found a significant relationship with
disturbance severity only. The high abundance of
TreM types such as bark pockets and bark shelters is
associated with insect outbreaks and the presence
of snags. The fall of trees caused by windthrows can
also cause superficial tree injuries leading to ex-
posed sapwood TreMs such as bark loss.
No significant effect was found for the rest of the
groups, which may be due in part to a lack of data
for TreM groups which are rare (twig tangles) or
not very common (rot-holes, exposed sapwood and
heartwood) in spruce forests, or there is no pre-
sumption of relationship with disturbances and
post-disturbance development.
Study Limitations
While our statistical analyses relied on established
approaches, our study has some limitations that
require mentioning. Firstly, while calculating the
disturbance history characteristics, we are not able
to distinguish between the drivers of disturbances
(wind or bark–beetle). Secondly, we are not able to
infer the most recent (cca 20–30 years) distur-
bances from tree cores; therefore, we calculated
them as a proportion of the current canopy open-
ness of standing dead trees, not taking in account
uprooted ones. Moreover, we only considered dis-
turbance events of maximum severity and time
since such an event; thus, if any disturbances of
similar severity occurred before or after the maxi-
mum severity event, their influence on TreM pro-
file was not taken into account. Lastly, the
disturbance history in this dataset dates back
approximately 250 years. The maximum time since
the most severe disturbance is 315 years. The
majority of data in this dataset is within the interval
of 0–250 years. Therefore, the 250–300-year
interval may be less reliable.
Implications for Conservation
and Management
Although our study focused on TreMs, our findings
are relevant for the conservation of many other
species. Primary forests are essential for providing
habitats for forest-dwelling species through high
richness and diversity of TreMs (Paillet and others
2018); however, their profile is dynamic and fol-
lows the long-term disturbance patterns. Distribu-
tion of highest TreM occurrence frequencies in
forest development phases changes between indi-
vidual groups, and therefore, the habitat availabil-
ity may change for different taxa. For example,
TreMs developed right after a disturbance event
such as insect galleries provide habitats for bats,
birds (Kameniar and others 2021), beetles and
other invertebrates (Bu
¨tler and others 2020). In the
mid-seral development stage, the highest TreM
density was observed for groups of concavities and
epiphytes that support various birds, amphibians,
rodents, mustelids or invertebrates. In the late-seral
phases and in low-severity disturbed plots, wood-
peckers and fungi—the TreM groups that occur
most frequently—enhance biodiversity itself but
also provide opportunities for secondary inhabi-
tants of cavities such as smaller birds, bats or par-
asites (Kraus and Krumm 2013; Robles and Martin
2014). Forest development driven by long-term
natural disturbances leads to the balanced distri-
bution of habitat availability in time in all forest
development phases across large scales (Thorn and
others 2017; Hilmers and others 2018; Mikola
´s
ˇand
others 2021). The mosaic of these different phases
1270 Veronika Zemlerova
´and others
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
at the forest scale then ensures the persistence and
diversity of species across forest landscapes, pro-
viding the primaeval remnants are large and
numerous enough to exhibit the majority of
developmental phases (Seidl and Turner 2022).
Our results thus show that all natural disturbance
severities (that is, high, moderate, and low) across
different time scales are necessary to maintain full
variation of TreMs and highlight the importance of
spatial and temporal scales to achieve the presence
and sufficient quality of biodiversity habitats.
CONCLUSIONS
Our results reaffirm the critical role of historical
processes in shaping landscape patterns of habitat
suitability for dependent and niche-specialised
forest organisms (Mikola
´s
ˇand others 2021). We
found that the fluctuation of disturbance activity
over long time frames is correlated with the
development, abundance and variety of available
microhabitats. Heterogeneous disturbance dynam-
ics maintain a constant supply and diversity of
TreMs at large spatial scales, leading to patchiness
in habitat availability which fosters high biodiver-
sity potential. We suggest that efforts to address
biodiversity losses in forests should focus on the
establishment and maintenance of complex, multi-
layered canopy structures, rather than solely on
species composition. The effect of disturbance
severity and timing on TreM groups differed sig-
nificantly among live and dead trees and particular
TreM groups, highlighting the importance of con-
sidering both the severity and timing of distur-
bances in assessing their impact on forest
biodiversity and TreM distribution. Thus, manage-
ment strategies, such as live-tree retention, de-
signed to enhance habitat for non-commercial
species (Kraus and Krumm 2013;Bu
¨tler and others
2013) will be unlikely to replicate levels of TreM
diversity that evolve as a consequence of complex
stand dynamics in natural systems, as demon-
strated here. We suggest efforts to address biodi-
versity loss in forests should focus on the
establishment of larger reserves or non-interven-
tion zones where natural processes and succes-
sional pathways predominate.
ACKNOWLEDGEMENTS
Funding for this research ‘‘Long-term disturbance
dynamics as a driver of abundance and diversity of
tree-related microhabitats in primary forests in
Europe’’ no. 80/2021 was provided by a project
financed from the OP RDE project Improvement in
Quality of the Internal Grant Scheme at CZU, reg.
no. CZ.02.2.69/0.0/0.0/19_073/0016944. Czech
Science Foundation (grant GACR no. 21-27454S).
M. Svitok was supported by the Operational Pro-
gramme Integrated Infrastructure (OPII), funded
by the ERDF (ITMS 313011T721).
FUNDING
Open access publishing supported by the National
Technical Library in Prague.
OPEN ACCESS
This article is licensed under a Creative Commons
Attribution 4.0 International License, which per-
mits use, sharing, adaptation, distribution and
reproduction in any medium or format, as long as
you give appropriate credit to the original author(s)
and the source, provide a link to the Creative
Commons licence, and indicate if changes were
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regulation or exceeds the permitted use, you will
need to obtain permission directly from the copy-
right holder. To view a copy of this licence, visit h
ttp://creativecommons.org/licenses/by/4.0/.
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