Ecological Applications, 24(4), 2014, pp. 663–679� 2014 by the Ecological Society of America

Disturbance, life history traits, and dynamics in an old-growth forestlandscape of southeastern Europe

THOMAS A. NAGEL,1,4 MIROSLAV SVOBODA,2 AND MILAN KOBAL3

1University of Ljubljana, Biotechnical Faculty, Department of Forestry and Renewable Forest Resources, Vecna pot 83,1000 Ljubljana, Slovenia

2Czech University of Life Sciences Prague, Faculty of Forestry and Wood Sciences, Kamycka 129,Praha 6 - Suchdol 16521 Czech Republic

3Slovenian Forestry Institute, Vecna pot 2, 1000 Ljubljana, Slovenia

Abstract. Much of our understanding of natural forest dynamics in the temperate regionof Europe is based on observational studies in old-growth remnants that have emphasizedsmall-scale gap dynamics and equilibrium stand structure and composition. Relatively littleattention has been given to the role of infrequent disturbance events in forest dynamics. In thisstudy, we analyzed dendroecological data from four stands and three windthrow patches in anold-growth landscape in the Dinaric Mountains of Bosnia and Herzegovina to examinedisturbance history, tree life history traits, and compositional dynamics. Over all stands, mostdecades during the past 340 years experienced less than 10% canopy loss, yet each standshowed evidence of periodic intermediate-severity disturbances that removed .40% of thecanopy, some of which were synchronized over the study area landscape. Analysis of radialgrowth patterns indicated several life history differences among the dominant canopy trees;beech was markedly older than fir, while growth patterns of dead and dying trees suggestedthat fir was able to tolerate longer periods of suppressed growth in shade. Maple had thefastest radial growth and accessed the canopy primarily through rapid early growth in canopygaps, whereas most beech and fir experienced a period of suppressed growth prior to canopyaccession. Peaks in disturbance were roughly linked to increased recruitment, but mainly ofshade-tolerant beech and fir; less tolerant species (i.e., maple, ash, and elm) recruitedsuccessfully on some of the windthown sites where advance regeneration of beech and fir wasless abundant. The results challenge the traditional notions of stability in temperate old-growth forests of Europe and highlight the nonequilibrial nature of canopy composition dueto unique histories of disturbance and tree life history differences. These findings providevaluable information for developing natural disturbance-based silvicultural systems, as well asinsight into maintaining less shade-tolerant, but valuable broadleaved trees in temperateforests of Europe.

Key words: Abies alba; dendroecology; Dinaric Mountains, Bosnia-Herzegovina; Fagus sylvatica;forest dynamics; intermediate severity disturbance; longevity; natural disturbance; old-growth forest; shadetolerance; species coexistence.

INTRODUCTION

After centuries of deforestation and soil degradation

in temperate forests of Europe, followed by widespread

planting of coniferous monocultures during the 20th

century, society is currently seeking ecologically based

forestry practices that maintain ecosystem services,

preserve native biodiversity, and enhance resilience to

climate change (Bengtsson et al. 2000, Spiecker 2003,

Schroter et al. 2005). Much emphasis has therefore been

placed on restoration of old-growth forest structure and

composition (Bauhus et al. 2009), the idea being to

create conditions under which native biodiversity

evolved, as well as promotion of complex age classes

and species mixtures at stand and landscape scales, a

strategy that may foster adaptation to future climate

changes (Noss 2001, Millar et al. 2007). Restoring such

conditions typically involves management approaches

that incorporate patterns and processes found in old-

growth forests, such as maintaining a sufficient supply of

dead wood (Christensen et al. 2005, Muller and Butler

2010) and harvesting schemes that emulate natural

disturbance processes and increase structural heteroge-

neity (Angelstam 1998, Seymour et al. 2002, Keeton

2006).

A major obstacle to developing such approaches for

the European temperate region, however, is the lack of

reference conditions where old-growth pattern and

process can be studied. Millennia of land use practices

have eliminated all but a few scattered remnants of old-

growth forest, which are primarily located in remote

mountain regions of eastern and southeastern Europe,

Manuscript received 5 April 2013; revised 11 September2013; accepted 13 September 2013. Corresponding Editor: E.Cienciala.

4 E-mail: tom.nagel@bf.uni-lj.si

663

where forests are typically dominated by mixtures of

beech (Fagus sylvatica) and fir (Abies alba). Much of our

current understanding of old-growth mountain forests

in Europe is based on early studies in these remaining

remnants (e.g., Leibundgut 1959, Zukrigl et al. 1963,

Korpel 1982, Mayer et al. 1989, Korpel 1995). The

conceptual model that emerged from this work suggests

that dynamics are driven by endogenous mortality of

canopy trees (i.e., small-scale gap dynamics), giving rise

to a steady-state system at stand scales, characterized by

a shifting, fine-scale mosaic of different stages of forest

development.

Recent work in many of these same old-growth forests

challenges this conceptual model, and highlights the role

of natural disturbances as a driver of ecosystem change.

Studies in old-growth beech and mixed beech–fir

communities of the Alps, Carpathian, and Dinaric

Mountains indicate that periodic intermediate-severity

damage from wind disturbances (i.e., single events that

cause stand-level damage ranging from scattered single

tree falls to larger openings several thousand square

meters in size) is an important component of the

disturbance regime in this region (Splechtna et al.

2005, Nagel and Diaci 2006, Nagel and Svoboda 2008,

Firm et al. 2009, Kucbel et al. 2010). Compared with the

continuous formation of small-scale gaps (e.g., ,100

m2), such disturbances play a key role in maintaining

biodiversity in temperate forest ecosystems by creating

biological legacies and increasing understory light levels

(Woods 2004, Hanson and Lorimer 2007, D’Amato et

al. 2008), and are likely to prevent forest stands from

reaching an equilibrium state (Frelich and Lorimer

1991, Woods 2000, 2004, Worrall et al. 2005). Although

empirical studies of disturbance regimes are increasing

in the temperate zone of Europe, it is still difficult to

make generalizations due to the lack of geographic

representation and methodological limitations. For

example, most recent research has examined disturbance

regimes by quantifying characteristics of recently formed

canopy gaps (Nagel and Svoboda 2008, Kucbel et al.

2010), an approach that covers a limited time span, or

with dendroecological data (Splechtna et al. 2005, Nagel

et al. 2007, Motta et al. 2011, Trotsiuk et al. 2012),

which allows reconstruction of disturbance patterns

several centuries past, but typically over a limited spatial

extent.

Furthermore, while these recent studies have yielded

valuable insight into disturbance regimes, few have

examined the role of disturbances on tree community

dynamics, particularly with regard to maintenance of

tree species diversity. In large part, our current

understanding of tree diversity in old-growth forests of

Europe is based on a floristic–phytosociological ap-

proach, whereby site conditions, rather than past

disturbances, are thought to control compositional

patterns (Braun-Blanquet 1964, Ellenberg 1988). Recent

research, however, suggests that intermediate-severity

disturbance in mixed beech–fir forests may be necessary

for canopy recruitment of more light-demanding species,

including maple (Acer pseudoplatanus), ash (Fraxinusexcelsior), and elm (Ulmus glabra) (Firm et al. 2009,

Nagel et al. 2010). What is lacking is a mechanisticunderstanding of community dynamics that links

natural disturbances and tree life history traits (e.g.,Lusk and Smith 1998, Bergeron 2000, Loehle 2000,Gutierrez et al. 2008). This is probably because there are

few empirical studies that quantify basic life historycharacteristics, such as shade tolerance, growth, and

longevity, of common temperate tree species in Europe(e.g., Kunstler et al. 2005, Petritan et al. 2007). Much of

what we know about shade tolerance and longevity, forexample, comes from early studies that relied mainly on

observational evidence (Ellenberg 1988, Korpel 1995).In this study we examined the disturbance regime, life

history traits, and compositional dynamics in an old-growth beech–fir forest landscape in the Dinaric

Mountains of Bosnia-Herzegovina. We used dendroeco-logical data to reconstruct patterns of disturbance in

four stands and three windthrow patches; by using aspatially explicit dendroecological approach that esti-

mates the area of past disturbances (Frelich andGraumlich 1994), we were able to reconstruct both the

frequency and severity of disturbances over the pastseveral centuries. Moreover, because our sampling wasdispersed over a relatively large area of old growth, the

results yield important information on stand andlandscape patterns of disturbance not captured by

previous dendroecological studies in the region. Weused the same dendroecological data set to provide

insight into interspecific differences in tree life historytraits, namely shade tolerance, growth rates, and

longevity. These data allowed us to address thefollowing questions relevant to the general understand-

ing of forest dynamics in the region. (1) Is thedisturbance regime consistent with the widely accepted

model of small-scale gap dynamics and fine-scaleuneven-aged stands of mixed mountain old-growth

forests in Europe? (2) Can interspecific differences intree life history traits, coupled with the reconstructed

history of disturbance, explain tree community compo-sition? Finally, we discuss how the results can informforest management in the temperate zone of Europe,

particularly in landscapes where maintenance of ecolog-ical functions is a management priority.

METHODS

Study area and sample sites

This study was conducted in the Peru�cica forestreserve in the Dinaric Mountains of Bosnia-Herzegovi-

na. With a size of ;1400 ha, Peru�cica is one of thelargest tracts of old-growth forest remaining in the

temperate zone of Europe. In the Dinaric Mountainregion, for example, most of the remaining old-growthforests are small (,100-ha) remnants (Diaci 1999),

making it difficult to capture the natural range ofvariability of disturbance processes. Thus, the large size

THOMAS A. NAGEL ET AL.664 Ecological ApplicationsVol. 24, No. 4

of Peru�cica allows a unique glimpse into natural

disturbances patterns and forest dynamics. The study

region is influenced by both mediterranean and conti-

nental climates, with a mean monthly temperature range

of �3.38C in January to 15.08C in July and a mean

annual precipitation of 1837 mm (Cemerno station,1305

m above sea level). Sampling was done between

approximately 1000 and 1400 m in elevation, where

beech and fir dominate the canopy layer. Several less

frequent species co-occur in the canopy, including

maple, elm, ash, and Norway spruce (Picea abies). The

forest has typical old-growth features, including large

amounts of standing and downed coarse woody debris,

heterogeneous stand structure, and large canopy trees

reaching heights between 40 and 50 m (Nagel and

Svoboda 2008, Nagel et al. 2010). Topography in the fir–

beech zone is characterized by deeply dissected, moder-

ate to steep slopes that surround the Peru�cica river

watershed. Soils are generally fertile and deep, derived

mainly from limestone and dolomite on the upper-

elevation slopes and a mixture of acidic sandstone and

shale at lower elevations (Fukarek and Stefanovic 1958).

The study region has certainly been influenced by

historic land use practices, but there is no evidence that

they were responsible for any of the patterns document-

ed in this study. In Peru�cica, there is no archival

evidence of historical cutting in the reserve (Fukarek

and Stefanovic 1958). In fact, more than half of the total

2 million ha of forests in Bosnia were characterized as

old-growth prior to the Austro-Hungarian rule begin-

ning in 1878 (Frohlich 1954). Given the low population

density in the region during the study period (Palairet

1997) and inaccessible nature of the terrain prior to the

road that was constructed in the 1950s, we have no

reason to believe that widespread cutting would have

occurred in Peru�cica. However, transhumant grazing

has probably occurred for centuries, but was mainly

limited to the alpine pastures above the forest reserve.

Our interviews with the few remaining shepherds still

practicing transhumance in the area suggest that sheep

and cattle rarely entered the forest, except under very

dry conditions when animals would use the forest edge.

Given that our plots were placed in the interior area of

the reserve, far from the alpine pastures that were used

for grazing, it is unlikely that historical grazing practices

influenced the study plots.

To capture landscape-scale patterns of disturbance

and the gradient in canopy composition encountered in

the study area, we divided the fir–beech zone into two

broad areas (Tunjemir and Zanoglina) located on

opposite sides of the watershed for sampling. Forest

structure and composition in the Tunjemir and Zano-

glina areas were extensively surveyed in a previous study

(Nagel et al. 2010), and can be summarized as follows.

The upper canopy (i.e., trees with dbh .30 cm) in

Tunjemir was dominated by beech (103 trees/ha),

whereas fir was less abundant (47 trees/ha). The upper

canopy in Zanoglina was mainly composed of fir (168

trees/ha) with a lower density of beech (44 trees/ha).

Maple, elm, ash, and spruce were sporadically distrib-

uted in the upper canopy layer in both areas at low

densities (i.e., ,3 trees/ha). Throughout both areas,

regeneration was sparse and dominated by beech; other

species had much lower densities (Appendix A).

Within each area, we used random coordinates to

locate two 1-ha plots (100 3 100 m), but restricted the

distance between the plots to at least 400 m (Fig. 1,

Table 1). In several cases, plots were shifted along the

slope contour to avoid sampling on intermittent streams

with steep banks. Additionally, during reconnaissance

for the four disturbance history plots, we encountered

several larger (�0.5 ha) windthrows (relative to the

smaller gaps that form regularly in the forest). These

patches were characterized by abundant tip-up mounds,

downed wood, and scattered windfirm canopy trees. We

selected three of the largest patches for further study

(Fig. 1, Table 1). Finally, throughout the entire beech–fir

zone, whenever we encountered a tree in the upper

canopy (typically .30 m in height) of a less frequent tree

species (i.e., maple, ash, and elm), we extracted an

increment core at a height of 1 m for growth pattern

analysis. The mean dbh measurements of the maple, ash,

and elm trees sampled in this study were 79 cm, 96 cm,

and 108 cm, respectively.

Field procedures

Disturbance history.—Disturbance history sampling

was conducted in 2006 and 2007 in the 1-ha plots. Each

plot was divided into 10310 m grid squares and the tree

stem (with dbh �10 cm) closest to the center of each

quadrat was cored at a height of 1 m and parallel to the

slope contour to avoid reaction wood. These trees were

later used for age structure analysis. If the closest stem

was not in the canopy, defined as trees receiving direct

sunlight from above, regardless of height (Lorimer and

Frelich 1989), the closest canopy tree to the quadrat

center was also cored. Canopy trees were used to

reconstruct disturbance history. When a tree was too

rotten to extract a useable sample, we were usually able

to obtain an intact sample at a higher coring height (up

to 2 m). In the few rare cases when the sample tree was

very decayed, we cored another stem of the same species

and of similar size within the quadrat. In quadrats

located under recently formed gaps with no trees of dbh

�10 cm, no core was taken. Rather, to provide

information on the recent history of disturbance on

the plots, we mapped the shape and position of canopy

gaps and snapped and uprooted trees with the aid of the

103 10 m grid. We also recorded the position of old pits

and mounds to supplement the dendroecological recon-

struction of disturbance. In total, we collected 582 cores

over the four plots for the analysis of age structure and

growth patterns.

Windthrow patches.—After delineating the approxi-

mate boundary of each windthrow patch, we established

three 625 m2 (25 3 25 m) plots separated by 10-m

June 2014 665EUROPEAN OLD-GROWTH FOREST DISTURBANCE

intervals along a transect oriented through the center of

each patch. Similarly, three 625-m2 plots were also

placed along a transect in a control stand adjacent to

each windthrow that did not show evidence of wind

damage. In each plot, the species and dbh of all live and

dead (standing and down) trees with dbh �5 cm were

recorded, as well as the number of seedlings (.0.5 m tall

but ,1.3 m tall) and saplings (.1.3 m tall but ,5 cm

dbh) of each species. To provide additional insight into

post-windthrow successional processes, in each wind-

throw plot we extracted increment cores from three to

five of the trees with dbh �5 cm nearest to the plot

center for each tree species present in the plots. Cores

were extracted at ;10 cm in height to help determine the

timing of tree establishment relative to each windthrow

event. No cores were sampled in the control areas.

To help characterize the disturbance history of each

windthrow patch, we recorded the species, dbh, and

stage of decay (following Nagel and Svoboda 2008) of

all snapped and uprooted boles in both windthrow and

FIG. 1. Map of the Peru�cica forest reserve in the Sutjeska National Park, Bosnia-Herzegovina; circles show the location of thefour disturbance history plots in Tunjemir (T1, T2) and Zanoglina (Z1, Z2); triangles show the three windthrow patches (Osoje,Tunjemir, Skakavac).

TABLE 1. Site and stand characteristics for the four old-growth Fagus–Abies plots and three windthrow patches in the Peru�cicaforest reserve, Bosnia-Herzegovina.

Characteristic

Disturbance history plots Windthrow patches

Tunjemir-1 Tunjemir-2 Zanoglina-1 Zanoglina-2 Osoje Tunjemir Skakavac

Map ID T1 T2 Z1 Z2 1 2 3Elevation (m) 1150 1200 1340 1400 1200 1240 1100Slope (8) 25–30 10–25 0–25 5–25 15–20 15–20 15–20Aspect (8) 40 40 240 260 340 350 360Size (ha) 1 1 1 1 0.5 .1.0 0.6Gap fraction (%) 17 43 22 27Canopy composition (%)

Fagus sylvatica 83 44 31 43 53 67 68Abies alba 17 56 69 57 40 30 32

Notes: Only the dominant two species, F. sylvatica and A. alba, are shown for canopy composition. The composition of thewindthrow areas is based on undisturbed control plots (see Methods: Windthrow areas). Size refers to the plot size for thedisturbance history plots and patch size for the windthrows.

THOMAS A. NAGEL ET AL.666 Ecological ApplicationsVol. 24, No. 4

control plots. Finally, in addition to the cores collected

within plots, we extracted increment cores from at least

three large, windfirm trees in the upper canopy within or

near each windthrow plot (;10 trees per windthrow

patch) to help date the disturbances.

Tree growth histories.—In addition to the reconstruc-

tion of age structure and disturbance history, we

examined patterns of tree ring growth indicative of life

history differences among the common tree species

found in the study area. This data set included all of the

increment cores from the 1-ha plots (N ¼ 582), the

windthrow patches (N ¼ 108), the less frequent tree

species encountered throughout the study area (N¼ 43),

and samples from additional ‘‘winner’’ and ‘‘loser’’ trees

of beech and fir cored in 2009 (N ¼ 121). We targeted

winners and losers to compare the growth history of

trees that reach the canopy with that of trees that die in

the shaded understory. Winners were defined as trees in

the lower part of the upper canopy (;20 m tall) in the

process of filling a gap. In other words, these were

intermediate-sized trees with crowns exposed to full sun

from above that were likely to grow into the upper

canopy. In contrast, loser trees were defined as the

largest recently dead or morbid trees (i.e., trees with

plageotropic growth and only a small amount of living

foliage) growing in the shaded understory and presumed

to be dead or morbid due to shading from above rather

than overcrowding. These trees typically had a dbh .5

cm and were ,20 m tall. Sampling was carried out in

four belt transects (;40 3 200 m) placed parallel to the

slope contour starting from the edge of each 1-ha plot

used for the disturbance history reconstruction. In each

transect, we extracted increment cores and recorded the

species and dbh for all winner and loser trees of both fir

and beech. Cores were sampled at a height of 1 m and

parallel to the slope contour. Over the four transects, we

collected 60 cores of beech and 61 of fir, with

approximately equal sample sizes of winners and losers

for both species.

Data analysis

Dendroecological procedures.—In the laboratory,

cores were dried, mounted, and sanded to a high polish

using standard procedures. Samples were then digitized

with the ATRICS system (Levanic 2007), and annual

ring widths were measured to the nearest 0.01 mm using

WinDENDRO software (Regents Instruments, Quebec,

Canada). The tree ring series were visually cross-dated

using marker years (Yamaguchi 1991) and by compar-

ison with a master chronology developed from a

drought-sensitive black pine (Pinus nigra) stand within

the same watershed as the study site (Poljansek et al.

2012). Cross-dating accuracy was verified with the

COFECHA program (Holmes 1983). We were not able

to successfully cross-date early portions of some samples

because of extended periods of very suppressed initial

growth. Such samples were nevertheless retained in the

analysis because they contained important information

on disturbance history and growth patterns. Most of the

cores either included or were less than 3 cm from the

pith (60%, ,1 cm; 85%, ,3 cm). For samples that did

not include the pith, the number of missing rings was

extrapolated from the curvature and average growth

rate of the innermost 10 rings (Duncan 1989).

Reconstruction of past disturbances.—Radial growth

patterns of all increment cores collected in the study

were analyzed for evidence of past disturbance events.

This analysis was used to construct disturbance chro-

nologies for the 1-ha plots and windthrow patches, as

well as to examine interspecific differences in tree growth

histories. Specifically, each core was checked for (1)

abrupt increases in radial growth (i.e., releases) and (2)

rapid early growth rates (i.e., gap-recruited trees), both

of which indicate mortality of a former canopy tree

(Lorimer and Frelich 1989). To determine if trees

qualified for gap recruitment, we defined species-specific

growth-rate thresholds as the 95th percentile growth rate

of suppressed trees sampled in the disturbance history

plots (Splechtna et al. 2005, Firm et al. 2009). This gave

a growth-rate threshold of 1.16 mm/yr for fir and 1.0

mm/yr for beech. Trees were considered gap-recruited if

the mean ring width of the initial 10 years of growth

exceeded the threshold value. In a few cases, trees that

did not meet the growth rate threshold, but had a

lifelong declining growth pattern, were also categorized

as gap origin (Lorimer and Frelich 1989). Gap

recruitment was only determined for cores that missed

the pith by less than 3 cm.

Releases were identified using the boundary line

technique (Black and Abrams 2003). The advantage of

this method is that it scales release detection according

to the pre-disturbance growth rate. Potential releases,

which are later scaled to species-specific boundary lines,

were identified by first calculating percentage growth

change values in each tree ring series with the running

mean method of Nowacki and Abrams (1997), which

compares consecutive 10-year growth intervals. The

maximum value of each growth pulse (pulses were

defined as positive, sequential percentage growth chang-

es values) was then selected as the potential release year.

To minimize the detection of short-term growth

responses caused by factors other than loss of canopy

trees, such as climate extremes or mast years, we only

used potential releases from pulses with percentage

growth change exceeding 50% (Splechtna et al. 2005,

Svoboda et al. 2012). These potential releases were

scaled relative to a boundary line constructed for both

fir and beech using tree ring measurements from all of

the increment cores sampled in the study (see Appendix

B for more detail on the species-specific boundary line

functions). Based on the original threshold of Black and

Abrams (2003), all releases within 20–100% of the

boundary line were tallied. Finally, to reduce the

number of falsely identified releases detected by the

boundary line, all releases for each sample were

subjected to additional visual inspection. Releases were

June 2014 667EUROPEAN OLD-GROWTH FOREST DISTURBANCE

deemed false if they lasted less than 10 years or were

caused by several narrow rings in a 10-year series, such

as growth reductions due to mast years of beech

(Drobyshev et al. 2010).

The release and gap recruitment events were used to

construct disturbance chronologies for each disturbance

history plot and windthrow patch. For the disturbance

history plots, the chronologies only included gap

recruitment events and growth releases indicative of

canopy accession (Lorimer and Frelich 1989). Namely,

only disturbance events that allowed trees access to the

canopy were included. The goal of this approach was to

exclude releases in existing canopy trees due to crown

expansion into a gap and moderate releases of under-

story trees caused by nearby gaps, because including

such events would overestimate the amount of canopy

area removed during a disturbance event. To distinguish

canopy accession events from releases in existing canopy

trees, we used species-specific diameter thresholds to

determine if a tree was in the canopy at the time of a

given disturbance event. Based on the approach of

Lorimer and Frelich (1989), data from the size structure

of canopy and understory trees in the disturbance

history plots were used to calculate the thresholds.

Releases were not counted for fir with dbh �28 cm and

beech with dbh �18 cm at the time of disturbance.

Following visual inspection of each tree ring series,

releases below these thresholds were counted as evidence

of canopy accession. When samples had multiple

releases of similar magnitude that met our criteria, each

release was tallied. We allowed for multiple releases

because understory trees often require several distur-

bance events to reach the canopy (Lorimer and Frelich

1989, Canham 1990).

Because canopy trees were cored at regular grid points

in the disturbance history plots, disturbance chronolo-

gies represent the area of the plots affected by new gap

formation in each decade, and were estimated by (x/

n)(100), where x was the number of trees showing a

canopy accession during a given decade and n was the

number of trees in the sample (Frelich and Graumlich

1994). To partially reduce the uncertainty in the

disturbance history interpretation due to the loss of

information farther back in time, we truncated chronol-

ogies when the sample size dropped below 10 trees

(Fraver et al. 2009). Furthermore, disturbance rates in

the last decade of the chronologies, 1990–1999, may be

underestimates because the method used to detect

releases requires a 10-year post-disturbance window,

and because trees recruited by disturbance events may

not have been large enough to core during the time of

sampling. For the windthrow patches, where we

collected a smaller number of cores, all gap recruitment

events and growth releases were included in disturbance

chronologies, regardless of canopy status.

Tree growth histories.—We quantified a variety of

lifetime growth characteristics that are indicative of tree

life history characteristics, namely, shade tolerance,

radial growth rates, and longevity. These included

statistics on periods of minimum and maximum growth

calculated from 10-year average growth periods (Orwig

and Abrams 1994) and the maximum duration of

sequential fast and slow growth per core, defined as

the number of consecutive years in which radial growth

was above (fast growth) or below (slow growth) species-

specific growth rate thresholds, calculated as the 75th

and 25th percentile ring widths, respectively, from all of

the ring width data for each species in the study (Baker

and Bunyavejchewin 2006). We also examined release

frequency and canopy accession patterns (i.e., gap origin

without a subsequent release; gap origin followed by one

or several releases; and non-gap origin followed by one

or several releases) among the dominant species. Life

span of the dominant species was estimated from the

90th percentile of age distributions of trees with dbh

.50 cm. When appropriate, calculations were only

carried out with complete cores, that is, cores that

included or missed the pith by less than 3 cm. All

dendroecological and statistical analyses were per-

formed in the statistical environment R (R Development

Core Team 2011).

RESULTS

Disturbance history.—Disturbance chronologies for

the four disturbance history plots show considerable

temporal variability in canopy loss over the past three

centuries (Fig. 2; Appendix C). Although there was no

clear evidence of stand-replacing disturbance, all of the

chronologies showed marked peaks, with maximum

canopy loss in a given decade ranging from 45% to 77%across the four plots. The mean rate of disturbance

ranged between 8.5% and 10% canopy area loss per

decade among the plots, yet the distribution of decadal

disturbance rates was skewed; with all plots pooled, 68%of decadal rates were below 10% canopy loss, 26%between 10% and 30%, 4% between 30% and 50%, and

2% greater than 50%. Therefore, the overall median

decadal rate of disturbance (5%) across the four plots

may be a better indication of the disturbance rate.

Rotation periods calculated from the pooled decadal

rates of all four plots (following Fraver et al. 2009)

provide an indication of the time needed for all plots to

experience a given disturbance rate: rates of �20%, 30%,

40%, and 50% canopy loss recur approximately every 90,

150, 200, and 460 years, respectively.

The age structures of the four plots were uneven-aged

and irregular, with pronounced peaks that roughly

followed periods with higher rates of disturbance (Fig.

3). For example, notable recruitment pulses followed

disturbance peaks in the 1660s and 1760s in Tunjemir 1,

the 1950s in Tunjemir 2, and the 1700s and 1820s in

Zanoglina-2. Recruitment dynamics of beech and fir

also show markedly different patterns among the four

plots. Some disturbance peaks were followed by

pronounced recruitment pulses of beech (e.g., the

1660s event in Tunjemir-1 and the 1950s event in

THOMAS A. NAGEL ET AL.668 Ecological ApplicationsVol. 24, No. 4

Tunjemir-2), whereas recruitment of both beech and fir

followed other disturbance peaks (e.g., the 1760s event

in Tunjemir-1 and the 1700s event in Zanoglina-2).

Windthrow patches.—Taken together, dendroecolog-

ical data (Fig. 4) and decay stages of windthrown trees

(Appendix D1) suggest that each of the windthrow

patches had a unique disturbance history. In Osoje,

most of the canopy was blown down in the 1950s

(increment cores indicate that the year of the event was

ca. 1956–1957), but a small disturbance peak in the

1930s, coupled with windthrown logs in two decay

classes, indicate that part of the canopy was already

damaged before the 1950s event. The Tunjemir site also

showed a pronounced disturbance peak ca. 1956–1957,

but there was little evidence of disturbance prior to this

event, and most windthrown logs were large beech trees

in the oldest decay class, indicating that the stand was

dominated by a closed canopy of beech prior to the

1950s event. The Skakavac site was mainly damaged by

an event in the 1990s, as indicated by a strong release

pulse and a large number of downed trees in the young

decay class, but a small release pulse in the 1950s and

FIG. 3. Distributions of recruitment ages (i.e., at 1 m tall) for trees sampled on a systematic grid in the four old-growth Fagus–Abies plots.

FIG. 2. Disturbance chronologies for the four old-growth Fagus sylvatica–Abies alba plots (corresponding to T1, T2, Z1, andZ2 in Fig. 1). Black and gray bars represent the percentage of canopy area disturbed as indicated by release (i.e., abrupt increase inradial growth) and gap origin (i.e., rapid early growth rate), respectively. Sample depth refers to the number of trees in thechronology in each decade. Chronologies were truncated when sample depth dropped below 10 trees.

June 2014 669EUROPEAN OLD-GROWTH FOREST DISTURBANCE

downed trees in several older stages of decay suggest the

canopy experienced some damage prior to the 1990s

event.

The structure and composition of the tree communi-

ties in each windthrow patch reflect these unique

disturbance histories. The windthrow in Osoje was

dominated by pole-sized (dbh 5–25 cm) beech trees

(Fig. 5), which established following the windthrow

events in the 1930s and 1950s (Fig. 4); shade-intolerant

tree species were very infrequent. Beech was also

considerably more abundant than in the neighboring

control area, where fir dominated the smaller diameter

classes. In contrast, the canopy layer of the tree

community in the Tunjemir windthrow was dominated

by less shade-tolerant species, mainly maple and ash

with dbh between 15 and 35 cm, whereas beech was

abundant in the 5–15 cm dbh class in both the

windthrow and control areas. All increment cores

collected from less shade-tolerant species indicated that

they established in the decades immediately following

the 1950s windthrow (Fig. 4). At the Skakavac site,

there was a dense thicket of seedlings and saplings,

primarily composed of beech and to a lesser extent

maple (Appendix D2), which probably developed in

response to the recent event in the 1990s. Beech was also

abundant in the 5–15 cm dbh diameter class; age data

indicate that this cohort established following the 1950s

event. Similar to the Osoje site, fir was abundant in

smaller diameter classes in the control area at Skakavac.

Tree growth histories.—There were a number of

significant differences in growth patterns among the

dominant tree species (Table 2), although determining

whether statistical differences arising from the large

samples in our data set are ecological meaningful is

challenging. Median radial growth and 10-year maxi-

mum and minimum growth periods were highest for

maple, followed by fir, and then beech, but the

differences between beech and fir were small. However,

fir had both the highest and lowest absolute growth rates

among the three dominant species. The median growth

rates of ash (1.38; N ¼ 8) and elm (1.19; N ¼ 6) were

similar to maple. Median values of the maximum

duration of consecutive fast and slow growth were

similar among beech, fir, and maple, although fir had

more skewed distributions compared to beech and

maple (Fig. 6). For example, the maximum duration

of fast and slow growth for fir reached 116 and 125

years, respectively, whereas beech and maple rarely

experienced consecutive fast or slow growth of .50

years. The pathway to canopy accession also differed

among beech, fir, and maple (Table 2). Maple was rarely

suppressed, reaching the canopy primarily through

canopy gaps (88%), whereas most of the beech (81%)

and fir (88%) trees experienced a period of suppressed

growth (with or without gap origin) prior to canopy

accession. Consistent with this pattern, fir had a median

of two canopy accession events per core, while the

median for beech and maple was one event.

FIG. 4. Disturbance chronologies (ascending bars) andrecruitment age structures (descending bars; the number oftrees in each age class for smaller trees cored at 10 cm height)for the three windthrow patches. Disturbance chronologies,represented by the number of trees showing release and gaporigin in each decade, were constructed from all increment coressampled within plots and large, windfirm canopy trees in eacharea. Note that for each species, we cored the stems closest toplot centers, so the age structures may not be representative ofthe actual proportion of each species in the windthrow patches.Rather, they are intended to give an indication of the timing ofestablishment of each species relative to past disturbances.Species shown in bars below the zero line are: Fagus sylvatica(beech), Abies alba (fir), Acer pseudoplatanus (maple), Ulmusglabra (elm), and Fraxinus excelsior (ash).

THOMAS A. NAGEL ET AL.670 Ecological ApplicationsVol. 24, No. 4

FIG. 5. Size structure (dbh class), by species, for the windthrow (left-hand panels) and neighboring control areas (right-handpanels). Note that vertical axes are on different scales with breaks inserted.

TABLE 2. Radial growth patterns of Fagus sylvatica (FS), Abies alba (AA), and Acerpseudoplatanus (AP); for median values, SD is given in parentheses.

Parameter FS AA AP

Number of samples 374 416 51Growth rate (mm/yr)

Median 0.75a (0.72) 0.78b (0.94) 1.12c (0.97)Median 10-year maximum 2.12a (0.88) 2.44b (1.39) 3.32c (1.16)Median 10-year minimum 0.24a (0.30) 0.24a (0.35) 0.50b (0.34)Absolute maximum 5.89 7.82 6.47Absolute minimum 0.07 0.05 0.24

Canopy accession pattern

Gap origin, no release (%) 19 11 88Gap origin, release (%) 34 31 3Non-gap origin, release (%) 47 57 9Median no. canopy accession events per core 1a (0.7) 2a (0.8) 1b (0.2)Median no. releases per core 2a (1.6) 2b (1.3) 1b (1.1)

Longevity (yr)

Maximum 523 345 35090th percentile 424 312 330

Notes: Sample sizes are lower for data on canopy accession patterns (FS¼ 222; AA¼ 202; AP¼32) and longevity (FS¼ 118; AA¼ 117; AP¼ 32). Medians in a row with the same lowercase letterare not significantly different; tests were done using a multiple comparison test after Kruskal-Wallis(P , 0.05) (Siegel and Castellan 1988).

June 2014 671EUROPEAN OLD-GROWTH FOREST DISTURBANCE

The growth rates of winner and loser trees also

provide valuable insight into life history differences

between beech and fir. Not surprisingly, growth rates

were higher for winners compared to losers for both

species (Table 3). Within the winner category, beech

generally had faster growth rates than fir, while growth

rates were similar between losers of the two species,

except for a faster median 10-year minimum rate for

beech. Overall, fir winners released more frequently than

beech winners, while losers of both species had a median

of one release per tree. Consecutive periods of fast and

slow growth differed between beech and fir (Fig. 6). For

FIG. 6. Distributions of the maximum duration of sequential fast and slow growth per core, defined as the number ofconsecutive years in which radial growth was above (fast growth) or below (slow growth) the species-specific growth ratethresholds. Panels show (A) slow and (B) fast growth for Fagus sylvatica (FS), Abies alba (AA), and Acer pseudoplatanus (AP), and(C) slow and (D) fast growth of F. sylvatica and A. alba winners (W) and losers (L). Winner trees in the lower part of the uppercanopy (;20 m tall) were in the process of filling a gap; loser trees were the largest recently dead or morbid trees (typically ,20 mtall, with dbh .5 cm) growing in the shaded understory. For details, see Methods: Field procedure: Tree growth histories. Boxesrepresent the interquartile range, and the horizontal line within the box shows the median. Whiskers extend to the 10th and 90thpercentiles and the points show outliers beyond the 90th percentile. The letters above the plots indicate significant differences (P ,0.05) based on multiple-comparison tests after Kruskal-Wallis (Siegel and Castellan 1988).

THOMAS A. NAGEL ET AL.672 Ecological ApplicationsVol. 24, No. 4

suppressed growth, the median period for fir winners

was nearly five times longer than for beech winners, and

suppression periods for fir losers were twice that of

beech losers. Among the losers, the longest period of

slow growth was 100 years for fir and 49 years for beech.

Interspecific differences were less pronounced for

consecutive periods of fast growth. Winners of both

species experienced longer periods of fast growth

compared to losers, and beech had longer periods of

fast growth than fir, although these differences were not

significant.

Estimated longevities were markedly different for

beech and fir (Table 2). The oldest beech trees were

.500 years old and large canopy dominants had a 90th

percentile age of 424 years, whereas fir did not exceed

350 years and had a 90th percentile age of 312 years. The

oldest maple was 350 years old (90th percentile, 330

years). Large canopy trees of ash and elm ranged from

253 to 331 (N ¼ 6) and 326 to 369 (N ¼ 3) years old,

respectively.

DISCUSSION

Disturbance regime.—The history of disturbance

during the past three centuries in the beech–fir stands

documented in this work exhibits substantial variability.

Although most decades experienced less than 10%

canopy loss, indicative of small-scale canopy distur-

bances (i.e., gap dynamics), all of the stands were

affected by periodic, intermediate-severity disturbances,

removing 20–50% of the canopy. Our data indicate that

rotation periods of disturbances spanning this range of

severity are 90 to 500 years, respectively. Although this

can only be treated as a rough estimate, as either a very

long time window or a large geographical area is needed

for accurate estimates (Frelich and Graumlich 1994),

these results suggest that intermediate-severity distur-

bances occur within the expected life span of a tree

cohort. Such disturbances are most likely to be related

to strong winds associated with intense, local thunder-

storms, one of the primary agents of disturbance in the

region (Nagel and Diaci 2006, Nagel et al. 2006, Nagel

and Svoboda 2008).

Although some of these events were only identified

within individual stands, there is evidence that somedisturbances were synchronized over the larger studyarea landscape. The four stands sampled for disturbance

history all show high rates of canopy loss from 1660 to1700, when most of the trees in the disturbancechronologies show evidence of gap origin (Fig. 2). This

was particularly pronounced in Zanoglina-2, wherethere were no trees that predated this period (Fig. 3).Although the sample depth was relatively low at this

time, the fact that all plots show a similar patternsuggests that there was an intense disturbance thatdamaged stands over the broader landscape. A wind-storm ca. 1956–1957 also caused widespread damage to

the broader study area, as indicated by the largedisturbance peak in Tunjemir-2 (damage to the canopyfrom this event is consistent with the high gap fraction in

this stand; Table 1 and Appendix E), several smallerpeaks in Tunjemir-1 and Zanoglina-1, and disturbancepeaks in the three windthrow patches.

Mortality patterns resulting from intermediate-sever-ity disturbances ranged from scattered, small gaps tolarger multi-tree openings and small patches of cata-

strophic damage (Appendices C and E). The 1950sstorm event well exemplifies the range of damage foundin the disturbance chronologies; this event removed

about half of the canopy trees throughout Tunjemir-1,creating a mosaic of interconnected gaps (Appendix E),and most of the canopy at the Tunjemir windthrow,

leaving only scattered, windfirm canopy trees. Theperiodic occurrence of intermediate-severity disturbanc-es found in this study is consistent with the emergingview that intermediate-severity wind disturbances are an

important component of the disturbance regime intemperate forests of Europe (Wolf et al. 2004, Nageland Diaci 2006, Nagel et al. 2007, Kucbel et al. 2010)

and North America (Frelich and Lorimer 1991, Green-berg and McNab 1998, Woods 2004, Fraver and White2005, Hanson and Lorimer 2007, D’Amato and Orwig

2008, Fraver et al. 2009, Stueve et al. 2011). Given thatevents in this range of severity probably have returntimes of about one to five centuries (Frelich and Lorimer

1991, Fraver et al. 2009) and damage trees at stand

TABLE 3. Radial growth patterns of winner and loser trees of Fagus sylvatica (FS) and Abies alba(AA); for median values, SD is given in parentheses.

Parameter

Winners Losers

FS AA FS AA

Number of samples 32 28 28 33Growth rate (mm/yr)

Median 0.80a (0.75) 0.55b (0.66) 0.40a (0.55) 0.40a (0.38)Median 10-year max 2.01a (0.68) 1.83a (0.84) 1.06a (0.68) 1.16a (0.34)Median 10-year min 0.34a (0.34) 0.17b (0.46) 0.18a (0.16) 0.13b (0.04)Absolute max 4.02 4.09 2.66 2.30Absolute min 0.10 0.09 0.08 0.09

Median no. releases per core 1a (0.9) 2b (1.2) 1a (0.8) 1a (0.9)

Note: See Table 2 for explanation of statistical tests. Different superscript lowercase lettersindicate significant differences.

June 2014 673EUROPEAN OLD-GROWTH FOREST DISTURBANCE

scales, we might expect a substantial portion of

temperate forest landscapes to be in some stage of

recovery from intermediate-severity wind damage

(Stueve et al. 2011).

Life history traits and community dynamics.—Our

dendroecological data are generally consistent with

earlier rankings of life history traits for European trees,

such as those from Ellenberg’s (1988, 1992) classic

studies, but there are some important differences that

warrant discussion. For example, Ellenberg character-

ized juvenile shade tolerance of beech and fir as very

high and maple as high, which is partly in accordance

with our findings; maple’s fast growth rate, limited

tolerance to suppression, and accession to the canopy

via gaps indicate that it is less shade tolerant than beech

and fir, which is in agreement with a recent study that

quantified the effects of shade on growth and mortality

of beech and maple (Petritan et al. 2007). However,

although the relative ranking of beech and fir regener-

ation as ‘‘very shade tolerant’’ may be reasonable, there

are several lines of evidence indicating that there may be

differences in their tolerance to shade during the pole-

size life stage. First, based on the size structure of trees

in the understory and those receiving direct light from

above in the four disturbance history plots, beech trees

with dbh ;10–20 cm were rarely growing in the shaded

understory, whereas fir trees in this size range were

frequently encountered beneath canopy cover. Second,

the growth pattern analysis of winner and loser trees

indicates that fir losers can tolerate substantially longer

periods of suppressed growth compared to beech,

whereas beech winners showed a trend toward faster

growth, longer periods of fast growth, and fewer releases

per core than fir winners. These patterns suggest that

there may be differences in the trade-off between

survival in shade and growth in gaps for these two

species, a trade-off often invoked to explain tree

coexistence in temperate forests (e.g., Kobe et al. 1995,

Pacala et al. 1996, Clark et al. 2010, Gravel et al. 2010).

However, without data on light levels or survival,

dendroecological data alone can only provide limited

insight into interspecific differences in shade tolerance.

We also found notable discrepancies between our

estimates of longevity and values reported in the

literature. Ellenberg (1988), for example, categorizes

the life span of beech and fir as intermediate (150–400

years) and maple as long lived (.400 years). Korpel

(1995), in his classic work on the ecology of old-growth

forests in the Carpathian region, gives estimates of 230

and 350 years for beech and fir, respectively, but these

were based on a small sample size. More recent studies

that report age structure data from old-growth beech–fir

stands in Bosnia-Herzegovina and Slovenia suggest

similar longevities for both species, at ;400 years (Firm

et al. 2009, Motta et al. 2011), and studies from old-

growth beech forests in the Italian Apennines and

Ukrainian Carpathians reported ages exceeding 500

years (Piovesan et al. 2005, Trotsiuk et al. 2012). Taken

together, our results and those of recent studies suggest

that beech may be longer lived than fir, which is very

much in contrast to the traditional forestry dogma in

Europe, which maintains that fir is substantially older

than beech. This thinking may stem from the large

diameter and height of adult fir trees; individuals .50 m

tall and with dbh .100 cm are not uncommon in old-

growth stands on productive sites, yet beech trees with

these dimensions would be exceptional.

Community dynamics observed in our study are

partly consistent with our results on disturbance history

and life history differences among the dominant tree

species, but not always. Based on shade tolerance alone

(and no dispersal limitation), we would expect higher

severity disturbances to promote recruitment of maple,

ash, and elm. Although we found partial support for this

in the three windthrow sites, the dynamics seem to be

more complex. For example, much of the current tree

canopy at the Tunjemir windthrow is dominated by

maple and ash that established after the 1950s wind-

throw event. In contrast, beech is much more abundant

than less shade-tolerant species at the Osoje and

Skakavac sites. Furthermore, fir was much less abun-

dant in the windthrow than in the neighboring control

areas at Osoje and Skakavac, where it dominated the

smaller diameter classes, lending further evidence that it

is capable of tolerating shaded understory conditions.

The different successional pathways found in the

windthrow patches seem to largely be the result of prior

disturbance, whereby low-severity canopy disturbance

before the last windthrow event (i.e., at Osoje and

Skakavac) enabled a bank of beech regeneration to

establish, which saturated the site and prevented the

recruitment of more light-demanding species even after

more widespread canopy removal. Such processes are

well documented in the stem exclusion stage of stand

development (Oliver and Larson 1996). Release of

advance, shade-tolerant regeneration following interme-

diate-severity disturbances, causing structural, but not

compositional change, has been documented in a

number of temperate forests (Webb and Scanga 2001,

Fraver and White 2005, Nagel et al. 2006, Beaudet et al.

2007, Fraver et al. 2009).

The presence of advance regeneration of beech and fir

may also explain the recruitment failure of less shade-

tolerant species within the four disturbance history plots

following the periods of heavy canopy removal.

Alternative explanations could be linked to a lack of

nearby adults (e.g., in the Tunjemir and Zanoglina

areas, average density of less tolerant species in the

canopy layer was ,3 trees/ha; Nagel et al. 2010). Our

sampling approach could have missed trees that

recruited to the canopy following past disturbances,

but died prior to the time of sampling, a common

problem with reconstructive studies that rely on static

age distributions (Johnson et al. 1994). Recruitment

patterns of beech and fir following the major distur-

bance peaks are also difficult to interpret; disturbance

THOMAS A. NAGEL ET AL.674 Ecological ApplicationsVol. 24, No. 4

peaks were followed by recruitment pulses dominated by

either beech, fir, or both species. It seems likely that

stand structure and composition at the time of these past

disturbances, coupled with the unique history of

disturbance in each stand, led to these variable

recruitment patterns. These results highlight the idio-

syncratic nature of forest dynamics at stand scales due to

the long-term legacy of past disturbances.

Among niche-based explanations of tree species

coexistence, differences in multiple tree life history

traits, expressed throughout all stages of a tree’s life,

are thought to contribute to maintenance of canopy

diversity (Nakashizuka 2001). In temperate forests, this

has been supported by both modeling work (Loehle

2000) and empirical studies (Veblen 1986, Lusk and

Smith 1998, Taylor et al. 2006, Gutierrez et al. 2008).

Several of these studies suggest that interspecific

differences in juvenile performance in gap–understory

gradients and adult life span contribute to tree

coexistence, whereby low recruitment rates of juvenile

trees into the canopy may be compensated by lower

mortality rates of adults. Although our analysis of radial

growth patterns only provides indirect evidence of

juvenile tree shade tolerance, the results suggest that

beech’s lower tolerance to shaded understory conditions

compared to that of fir may be balanced by the longer

life span of beech. In addition to life span, growing tall

may also convey certain advantages, namely, permanent

access to light, while casting shade on shorter neighbors

(Loehle 2000). Adult fir trees, which often reach heights

.50 m in mature stands, form an emergent canopy over

neighboring beech trees, thus adding another dimension

to the possible life history strategies that contribute to

maintaining tree diversity in beech–fir forests (Szwagrzyk

et al. 2012).

Although various life history differences may contrib-

ute to equilibrium coexistence of beech–fir forests at

stand scales, the relatively frequent occurrence of

intermediate-severity disturbances found in this study

suggests that canopy composition is probably non-

equilibrial. Certainly, the persistence of less shade-

tolerant species in our study system, such as maple,

ash, and elm, is linked to disturbances that create

canopy openings larger than those formed from

‘‘background’’ mortality of single canopy trees. Previous

work in Peru�cica indicated that maple, for example,

requires gaps of at least 400 m2 to recruit to the canopy

(Nagel et al. 2010). Once these less shade-tolerant

species reach the canopy, their relatively long life span

and seed dispersal ability may ensure their persistence in

the stand, particularly if intermediate-severity distur-

bance recurs at intervals suggested by our data. The

presence of these less shade-tolerant species in beech-

dominated forests of Europe has typically been associ-

ated with more mesic site conditions (Ellenberg 1988);

our results emphasize that disturbance, not only site

conditions, may be an important mechanism by which

these species coexist. Finally, our results and those of

other recent studies highlight that gap-phase models of

community dynamics, whereby tree diversity is main-

tained via tree replacement under a regime of low

intensity, relatively continuous canopy mortality (e.g.,

Forcier 1975, Barden 1980, Runkle 1982, Woods 1984),

may not be sufficient to explain the dynamics of tree

communities in temperate forests without considering

the influence of periodic, intermediate-severity distur-

bances (Woods 2000, Beaudet et al. 2007, Firm et al.

2009).

Management implications.—Throughout mountain-

ous regions of Europe, where beech and mixed beech–

fir forests are common, forests are managed with various

even- and uneven-aged silvicultural systems, including

single-tree selection, group selection, and shelterwood

systems (Madsen and Hahn 2008, Brunet et al. 2010,

Boncina 2011b). Used individually, none of these

systems would be sufficient to emulate the spatial and

temporal variability of canopy mortality documented in

this study. Rather, harvesting that employs several

silvicultural systems at appropriate spatial and temporal

scales within a forest landscape would be required to

reasonably mimic natural mortality patterns and to help

foster structural and compositional diversity at land-

scape scales (Seymour et al. 2002, Hanson and Lorimer

2007). For example, in mixed beech–fir forests managed

with small-scale selection silviculture, an approach that

is often advocated in such forests types in Europe

(Boncina 2011b), periodic, spatially variable harvests

that remove ;20–50% of the upper canopy layer in

patches several hectares in size could mimic the

intermediate-severity disturbances documented in this

study. Such structures may be best achieved with an

irregular shelterwood system (Raymond et al. 2009). In

other temperate forest regions where intermediate-

severity wind disturbances periodically interrupt forest

dynamics driven by small-scale, ‘‘background’’ mortal-

ity, similar approaches have been recommended to

curtail diversity declines that may result from only using

small-scale selection systems (Woods 2004, Hanson and

Lorimer 2007). Clearly, care needs to be taken not to

over-disturb managed landscapes, given that some

amount of natural canopy disturbance is inevitable,

such as damage from catastrophic windstorms (Seymour

et al. 2002).

Although long-term use of single-tree selection is

likely to result in a loss of less shade-tolerant species

(Schutz 1999), periodic higher intensity cutting, through

group selection, shelterwood cuts, or other more

irregular multi-cohort systems (Raymond et al. 2009),

should help to maintain tree diversity. However, our

results caution that advance regeneration of shade-

tolerant species, in our case beech, may inhibit

recruitment of less shade-tolerant species following

heavier harvests. This is particularly relevant for the

application of group selection and shelterwood systems,

which tend to favor shade-tolerant advance regeneration

by establishment and expansion of group openings in

June 2014 675EUROPEAN OLD-GROWTH FOREST DISTURBANCE

areas where beech regeneration is already established or,

in the case of shelterwood systems, by waiting for a mast

year to promote the establishment of dense beech

regeneration prior to the final overstory harvest. To

facilitate recruitment of less shade-tolerant species, it

may be necessary to use periodic, heavier cuts in closed-

canopy areas devoid of shade-tolerant advance regener-

ation, but where adequate seed sources of less shade-

tolerant species are present.

In addition to silvicultural prescriptions that account

for the size and frequency of natural disturbances,

incorporating other biological legacies resulting from

disturbances, particularly coarse woody debris, is central

for developing ecologically based management systems.

In forests dominated by beech, for example, the

importance of large old trees and sufficient amounts of

dead wood for maintaining myriad species dependent on

these structures is well documented (Brunet et al. 2010,

Gossner et al. 2013). Periodic, intermediate-severity

disturbances, similar to those documented in this work,

result in pulses of dead wood input in old-growth forests

(D’Amato et al. 2008), and are likely to play an

important role in the population dynamics of species

dependent on these structural elements (Jonsson et al.

2011). For example, a conservative estimate of the

amount of dead wood added to the Tunjemir-2 plot

following the single windthrow event in the 1950s totals

about 240 m3/ha (i.e., 50 trees with mean dbh of 64 cm),

more than an order of magnitude greater than the

average amount found in managed forests of Europe

(Forest Europe, UNECE and FAO 2011). Creating

pulses of dead wood input in managed forests, however,

is challenging, but could involve retaining a portion of

felled trees during a harvest, creation of dead wood

islands within a matrix of managed forest (Jakoby et al.

2010), or limiting the amount of salvage logging

following natural disturbances in managed areas.

Indeed, many of the findings documented in this work

would be challenging to incorporate in forests where

wood production is a primary function. Large amounts

of dead wood retention, long rotation periods (e.g., the

canopy residence time, calculated from the inverse of the

overall median disturbance rate, is 200 years in our

study area), and landscape-scale structural heterogeneity

may be unrealistic goals throughout much of the

European temperate region, where forest areas are often

small and heavily utilized. Despite these challenges, the

idea that managing forested landscapes with ecologically

based forestry (often termed ‘‘close-to-nature’’ forestry

in Europe) supplants the need for a segregated approach

to forest management, whereby forest land is divided

into areas focused on intensive wood production and

protected areas focused on ecological functions, is

gaining increased attention in Europe (Boncina 2011a).

However, we caution that close-to-nature forestry

should not be treated as a panacea for forest manage-

ment; in addition to forest land managed with ecolog-

ically based approaches, there is still a need to protect

and expand unmanaged forest reserves in the temperate

region of Europe to create large areas of old-growth

forest where landscape-scale structural and composi-

tional heterogeneity can develop. Recent work, in fact,

suggests that triad forest management (Seymour and

Hunter 1999), consisting of an intensive management

zone focused on wood production, an integrated

management zone that balances ecological and econom-

ic functions (e.g., similar to close-to-nature forestry in

Europe), and a reserve zone for restoration or protection

of existing old-growth forest, may be a better approach

to biodiversity protection than a less intensive integra-

tion approach spread out over a forested landscape

(Montigny and MacLean 2006, Tittler et al. 2012). The

more balanced approach of the triad model should also

provide more flexibility to foster adaptation to climate

change (Millar et al. 2007).

ACKNOWLEDGMENTS

Funding was provided by the Slovenian Research Agency(bilateral, program financing) and the Pahernik Foundation. M.Svoboda received support from the project ESF and MSMTCZ.1.07/2.3.00/30.0040. We thank the staff at Sutjeska NationalPark for allowing us to carry out research in the Peru�cicareserve. For help in the field and laboratory, we thank MatejTajnikar, Urban Oroz, Janez Miklavcic, Katarina Flajsman,Gal Fidej, Urska Bradesko, Urska Klepec, Tihomir Rugani, andJan Nagel. We thank Jeri Peck, Robert S. Seymour, and twoanonymous reviewers for providing valuable comments on aprevious version of the manuscript. Finally, we thank KerryWoods for many stimulating discussions on disturbance andcommunity dynamics in temperate forests.

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SUPPLEMENTAL MATERIAL

Appendix A

Forest structure and composition of the Tunjemir and Zanoglina areas in the Peru�cica forest reserve (Ecological ArchivesA024-039-A1).

Appendix B

Plots of percentage growth change values with respect to prior growth for annual growth increments of Abies alba and Fagussylvatica, including the boundary line functions for both species (Ecological Archives A024-039-A2).

Appendix C

Animations showing the spatial and temporal patterns of canopy accession (including both gap origin and release) in the fourdisturbance history plots (Ecological Archives A024-039-A3).

Appendix D

Number of gapmakers in different decay classes for Fagus sylvatica and Abies alba and density of seedlings and saplings in thethree windthrow and neighboring control areas (Ecological Archives A024-039-A4).

Appendix E

Maps of canopy gaps for the four disturbance history plots (Ecological Archives A024-039-A5).

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