Plant Ecol (2014) 215:1067–1080
DOI 10.1007/s11258-014-0365-4
Regeneration of oaks (Quercus robur/Q. petraea) and three
other tree species during long-term succession
after catastrophic disturbance (windthrow)
Frank Götmark • Charliene Kiffer
Received: 2 May 2014 / Accepted: 29 May 2014 / Published online: 17 June 2014
Ó Springer Science+Business Media Dordrecht 2014
Abstract In broadleaved temperate forests in Europe, oak (Quercus robur/Q. petraea) regeneration is
reported to be weak or absent. However, most work
concern seedlings or saplings, studied relatively few
years. We studied a Picea abies stand in Sweden,
windthrown and logged (all stems harvested) in 1969,
testing the hypothesis that oaks regenerate in the long
term among competing tree species after catastrophic
disturbance. In 2011, after 40 years/growth seasons,
we recorded live and dead trees in the new stand and
investigated the surroundings, competition, and succession. The following trees, up to 26 m tall, colonized: Sorbus aucuparia, Betula pendula/B.
pubescens, Fagus sylvatica, Q. robur/Q. petraea,
and Corylus avellana (a shrub). Betula dominated,
and only Fagus was regenerating in 2011. Sorbus had
produced most of the dead trees, mainly or partly
through intraspecific competition. In the stand, compared to the surroundings, Quercus, Picea, and Alnus
glutinosa were under-represented, and Sorbus, Betula,
and Fagus were over-represented. Yet, the density of
Quercus was far from negligible; 48 large trees/ha.
Most of the oaks (74 %) were co-dominant trees and
Communicated by J. D. A. Millington.
F. Götmark (&) C. Kiffer
Department of Biological and Environmental Sciences,
University of Gothenburg, Box 463, 405 30 Göteborg,
Sweden
e-mail: [email protected]
many grew near Sorbus. Thus, oaks can survive and
grow fast among pioneer trees and browsing animals, a
conclusion which is supported by the literature (nine
studies identified). High mortality of Sorbus is part of a
long-term succession, where Fagus might come to
dominate. However, Quercus likely will persist, in low
density. We propose three key traits contributing to
long-term persistence of Q. robur/Q. petraea in
European temperate forests: long life span, ecological
plasticity, and resistance to disturbances.
Keywords Quercus Forest Woodland Trees Disturbance Succession Competition
Introduction
In temperate forests, large oaks (Quercus spp.) are
prominent and may be considered as foundation
species, exerting an impact on community properties
disproportionate to their abundance (Lindbladh and
Foster 2010). Individual oaks may become more than
900 years old and large oaks are valuable for timber,
biodiversity, and esthetics (Tyler 2008; Johnson et al.
2009; Lindbladh and Foster 2010). Retaining oaks in
ecosystems requires adequate regeneration, but it is
generally considered poor in the northern hemisphere,
and may be insufficient in the long run to maintain the
populations (Lorimer et al. 1994; Kelly 2002; Oliver
et al. 2005; Harmer and Morgan 2007; Brudvig and
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Asbjornsen 2009). Depending on stand and treatment/
disturbance, oaks regenerate by seeds (acorns),
advance regeneration, and sprouts from stumps and
stems (Jones 1959; Johnson et al. 2009).
Poor oak regeneration seems to be caused by many
factors. Browsing of small oaks by increasing populations of ungulates is one negative factor (e.g.,
Kullberg and Bergström 2001; Healy 2003) and
insufficient light and/or competition in mixed forests
under secondary succession is another factor—oaks
are not as shade-tolerant as many other trees and
shrubs (Lorimer et al. 1994; Götmark 2007; Brudvig
and Asbjornsen 2009). But most studies of oak
regeneration cover fewer than 10 years and the oaks
may then still be small, often less than 1 m tall. Forest
succession is a slow process, and may be interrupted
by natural and cultural disturbances in the landscape.
Several catastrophic windstorms recently hit western Europe and damaged many forests (Nilsson et al.
2004; Schütz et al. 2006). The storms usually come in
the winter (Nilsson et al. 2004), and coniferous trees
are windthrown to a larger extent than deciduous trees.
Salvage logging of windthrown trees is common
(review in Lindenmayer et al. 2008). Natural regeneration after such logging might contribute to conversion to broadleaved stands (e.g., Harmer and Morgan
2009; Vodde et al. 2010; Jonasova et al. 2010), but
long-term studies of stand development after salvage
logging are rare.
Studies of tree colonization on bare ground after
salvage logging, or on any cleared forest land which is
not artificially regenerated, can provide critical tests of
regeneration of oaks and other trees. One classical
study, ‘‘Forty years of change in Lady Park Wood’’
(Peterken and Jones 1989) describes regeneration of
trees and shrubs in a clearing 1943–1983, including
some oak regeneration (see below). Here, we present a
related long-term study; forty years of change in
Labbra Park Wood, the site of a former Picea
plantation in southern Sweden, completely windthrown during the storm Ada in September 1969. It
was the strongest storm in Sweden between 1900 and
2000 (Schlyter et al. 2006) and damaged about 37
million m3 of stem wood. We test the hypothesis that
oaks [Quercus robur L./Q. petraea (Mattuschka)
Liebl.] regenerate among competing tree species after
catastrophic disturbance, under non-intervention and
in the long term. In addition, we ask what factors in the
current stand, in its history, and in the surroundings,
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Plant Ecol (2014) 215:1067–1080
influenced oak regeneration? Because the stand had
high stem density and contained three other tree
species that were abundant, we focus on the success
and ecology of four species (including oak). In doing
so, we also present new information on Sorbus
aucuparia L., which may be the most widespread tree
species in the Palearctic region. In 2011, we examined
tree species composition in Labbra Park Wood, and
analysed aspects of dispersal, growth, competition,
and succession. To judge the success of individual
oaks in the stand, we analysed their crown and stem
positions. The results, combined with earlier studies,
suggest three key traits of Q. robur/Q. petraea that
may explain the long-term success of these trees in
Europe (Lindbladh and Foster 2010).
Methods
Study area and history
The forested Labbra Park Wood is located on a
peninsula (N57°39.80 , E12°4.90 ) east of Gothenburg in
SW Sweden, in the temperate (boreonemoral, or cold
temperate) zone with naturally occurring deciduous
broadleaved tree species (Nilsson 1997). The study
site and forest stand (Fig. 1) are protected as nature
reserve. The mean temperature (1961–1990) for
January was -0.5 °C and for June was 14.5 °C; the
mean precipitation for January was 80 mm and for
June 70 mm (see www.smhi.se). Southwestern Sweden is lowland (\300 m above sea level) with mainly
gneiss and granite, sometimes exposed, in a mosaic
landscape of forest, fields, wetlands, and lakes. Forest
covers about 60 % of the land area. The forests and
forestry are dominated by production stands of P.
abies [(L.) Karst] (50 % of standing volume) and
Pinus sylvestris L. (30 %); other tree species are
mainly birch Betula pendula Roth/B. pubescens Ehrh.
(about 10 %); also Populus tremula L., Q. robur/Q.
petraea, Alnus glutinosa [(L.) Gaertner, Fagus sylvatica L., Sorbus aucuparia L. and other tree species
occur in the landscape.
The study site was dominated by agriculture
130 years ago (grazing and hay meadows). Picea
was planted in 1882 (archives for Råda Säteri,
Landsarkivet, Gothenburg) and the trees ‘‘had a mean
height of more than 40 m’’ in 1963 (historical
document at Härryda municipality). A photograph
Plant Ecol (2014) 215:1067–1080
1069
S
B
B
Fig. 1 The study site in SW Sweden, with P. abies windthrow
in 1969 marked with solid line, and the studied plot marked with
dashed line. The new, young stand is visible as smaller crowns
in the surrounding forest, which is mainly composed of
deciduous broad-leaved trees. The circles at B show three large
(old) beeches, the ones that are closest to the windthrow. S
indicate a group of Picea (somewhat younger than the
windthrown Picea). The light tree canopy around the windthrow
are large oaks defoliated by larvae of moths in this particular
year (2005, June—6 years before our study)
from a distance in 1950 shows a dense stand with tall
Picea (own archives, F.G.). Many large, partly
decomposed spruce stumps remained in the stand in
2011, but no stumps of broadleaved trees. The
windthrow, 2.5 ha, lies below a hill on a north-facing
slope (Fig. 1). The soil is till, influenced by postglacial sea (Magnusson 1978). The former Picea stand
probably caused podzolization, but brown earth soils
now dominate the site, silty—fine sandy, with a small
(1 % or less) clay component. The summer herb flora
in 2011 was sparse due to low light level under closed
canopy, but in spring 2011 [50 % of the ground was
covered with Anemone nemorosa L.
After the storm on 22 September 1969, all Picea
were removed from the site by tractors (in March–
April 1970; property documents, Härryda municipality). This caused much ground and soil disturbance.
Also remaining high stumps from broken Picea trees
were cut and removed. Several uprooted Picea stumps
were put back in normal position, according to the
instruction—some mounds remained in 2011. No
Picea logs were left. A few scattered standing larger
broadleaved trees were left in the windthrow and
identified by us (see below). The stand and the
peninsula was managed under a 25-year legal conservation agreement from 1963 onwards (‘‘Naturvårdsavtal Näset Råda Säteri,’’ dated 12 November 1964,
Härryda municipality), and no planting, pre-commercial thinning, or other forestry activities took place
after the windthrown trees were harvested. The storm
came just after Quercus normally drop acorns, and the
disturbance of soil and litter may have contributed in
hiding them (Quercus occurred in stand and plot, see
below). We assume that most of the oaks regenerated
from seeds, although it is possible that advance
regeneration also existed in 1969 (e.g., oaks shorter
than 1 m).
Browsing animals at the site include hare, Lepus
timidus L. and L. europeaus Pallas (permanent populations), roe deer Capreolus capreolus L. (permanent
population), and moose Alces alces L (visiting individuals). The roe deer and moose populations
increased in Sweden from about 1960 onwards
(Cederlund and Liberg 1995). The Swedish Association for Hunting and Wildlife Management compiles
county-wise bag records for these species, and we
obtained annual data for 1960–1994 (from J. Kindberg). We used data for 1974–1984, the approximate
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period when browsing ungulates could have affected
small trees in the plot (see below), and three counties
surrounding the study site (‘Göteborgs och Bohus län’,
southern part of the former ‘Älvsborgs län’, and
‘Hallands län’). During these years, 82,540 roe deer
and 60,092 moose were shot in the counties, and bag
records increased each year. The mean annual number
of shot roe deer per km2 of forest land was 0.80, and
the mean annual number of moose shot per km2 of
forest land was 0.58 (1974–1984, n = 11 years).
Good estimates of roe deer population density were
reported from Bogesund (390 km NW of our site) over
many years (Kjellander et al. 2004: Fig. 1). Based on
their data, hunted populations vary in density between
5 and 15 roe deer per km2, but densities also depend on
forage and habitat conditions (Cederlund and Liberg
1995). Based on the description in Kjellander et al.
(2004), the productivity of the land in Bogesund
should be lower than in our area. Moreover, our study
site on the peninsula is, and was part of a large manor
(’Råda säteri’) with a lower hunting pressure
1970–1990 than in other forests nearby, so the local
density of ungulates at the site was probably somewhat
higher compared to the surroundings (Conny Samuelsson, local experienced hunter, pers. comm. 2014).
Therefore, we judge that the density of roe deer during
1974–1984 was about 10–15 per km2, which we refer
to below as ‘‘intermediate density.’’ The moose
population density was lower and hard to estimate,
but moose visited the site regularly (Conny Samuelsson, pers. comm.).
Plot and sampling
The 1.32 ha study plot covered a large part of the
windthrow (Fig. 1) and was divided into 29 rectangular subplots (size 300–500 m2). Field work was
conducted in spring 2011 (late March–early May)
and January 2014. In the subplots, for living trees taller
than 1.3 m in height, we recorded species, height, and
stem diameter at breast height (1.3 m = dbh). For
Picea, we recorded also trees (seedlings) that were less
than 1.3 m tall. Picea is the most common tree in
Sweden, shade-tolerant, and its ‘‘invasion’’ into oak
habitat is often debated. Data for the two similar
Quercus species, and for the two similar Betula
species, were pooled; all four species were recorded,
but intermediate forms made it difficult to separate
them.
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Dead trees indicate mortality rates for the species
competing with oaks, and for oaks too. We measured
the diameter and the length of fallen trees and dead
wood pieces more than five cm in diameter. Dead
wood lying over two or more subplots was subdivided
among these subplots. Standing dead trees were
recorded separately. The dead wood was classified as
either hard or soft (a knife could be put in more than
1 cm into the wood). We measured dead wood in 20
subplots, distributed over the plot with 29 subplots
(due to shortage of time, all 29 subplots could not be
studied).
Some large trees appeared to be older than 40 years
and having survived the storm standing. They were
cored at tree base using an increment borer (Haglöfs,
Sweden), and we prepared and sanded the cores to
determine the age from tree rings, and to estimate
diameter of the trees in 1969.
To examine the role of surrounding trees for tree
colonization, we compared species composition in the
plot in 2011 with that of the forest adjacent to the
windthrow. We measured diameter (dbh) of all trees
within 20 m of the approximate edge of the windthrow
(Fig. 1). Then we included only those trees that we
judged were alive and mature in 1969. Our judgements
were done after we had cored trees and estimated their
ages—this made it easier to exclude too young trees
(they were a minority; mainly Fagus). In the analysis,
we compared the adjacent forest (referred to as
‘‘outside’’) with the plot (windthrow) and calculated
the sum of basal area of trees outside, and in the plot.
We measured a total basal area of 30.1 m2 outside, and
40.2 m2 within the plot, and added trees that survived
the storm in the plot (see below) to the mature trees
outside, as these also could be seed trees. For our
comparison, we used the percentage basal area of the
tree species outside, versus percentage basal area of
the tree species within the plot.
To assess the status of new oaks in the plot and the
role of stems/species near them, we studied 54 oaks
sampled along three fixed transects through the stand
in January 2014 (referred to as focal oaks below). We
classified oak crowns in four classes (Nyland 2002,
pp. 386–389): dominant trees would have C50 % of
their crown above the co-dominant trees that form the
main canopy in an even-aged stand (cf. Nyland 2002);
lower intermediate trees had 5–25 % of their crowns
in the crown layer of co-dominant trees; and smaller
overtopped trees no part or\5 % of their crown in the
Plant Ecol (2014) 215:1067–1080
Table 1 Variables used in
the stepwise multiple
regression model, based on
sampling of subplots at
Labbra Park Wood, SW
Sweden
1071
Mean
(m3/ha)
SD
Range
n (no of
subplots)
Volume, dead wood of Sorbus intermedia
20.0
14.1
45.8
20
Explanatory
Volume, living Betula (Betula pubescens/B.
pendula, pooled)
167
62.7
220
20
Volume, living Fagus sylvatica
63.0
52.2
224
20
Volume, living Sorbus aucuparia
60.2
30.2
111
20
Variable
Dependent
crown layer of co-dominant trees. At each focal oak,
we recorded the species of the three nearest stems
taller than 8 m (to exclude smaller regenerating
Fagus, see below). The few older oaks that survived
the storm were excluded from the crown classification.
The main species in the stand (Quercus, Betula,
Sorbus, Fagus) and Picea are referred to by genus name
below, including also hazel Corylus avellena L., which
is a tall shrub that we only included in stem counts.
Calculations and statistics
For live trees, we estimated volume (including bark)
for Betula from the equation given in Brandel (1990).
For Quercus and for Fagus, we used the equations
given in Hagberg and Matérn (1975). For Sorbus, we
are not aware of any volume function. The stem/tree
form of Sorbus and sallow Salix caprea L. generally
resembled that of Betula in the stand, and we used the
Betula equation also for Sorbus and Salix. For fallen
dead wood, we calculated volume from the equation
for a cut cone (frustum of a cone), while for standing
dead trees, we used the same equation as for live
specimens of the species (most standing dead trees
were still fairly intact).
For the plot as a whole, we compared size of species
by frequency distributions of stem diameter sizes
(5 cm-intervals) and tree heights (5 m-intervals). For
statistical comparisons among species, we calculated
confidence intervals, as recommended by Johnson
(1999) for cases, where they are possible to use. For
cored trees, we present ages and diameters, or the
absence of these trees, in 1969.
The subplots were used to facilitate recording, to
examine variability within the new stand (CV, coefficient of variation; standard deviation divided by
mean value), and to analyse aspects of competition
related to stand dynamics and oak regeneration. We
expected that Sorbus, being a smaller tree than Betula,
Quercus, and Fagus (Zerbe, 2001), should have
suffered in competition from the other trees during
the 40-year period. The stand contained much dead
wood of Sorbus (see below), and its dieback may have
influenced the success of oaks. We predicted that dead
wood of Sorbus in subplots (n = 20) should be
positively correlated with living volumes of Betula
and Fagus in subplots (Betula and Fagus dominated
the stand). Alternatively, dead wood of Sorbus should
be positively correlated with living volumes of Sorbus,
if intraspecific competition (self-thinning) was the
major factor. To test these alternatives, we used
stepwise linear multiple regression in PASW Statistics
18.0 (release 18.0.2 for MacIntosh, IBM 552 Corporation, NY, USA http://www.spss.com.), with dead
wood volume of Sorbus in subplots as response variable, and living volumes of Betula, Fagus, and Sorbus
as three explanatory variables (Murtaugh 2010). The
results of regression models are sensitive to the range
of variables (Götmark et al. 2011)—here dead wood
volume of Sorbus, and living volume of Betula, Fagus,
and Sorbus. Table 1 shows the large variability and
range of the variables, making the analysis meaningful. These variables had no serious collinearity (pairwise r B0.6), which was confirmed by relatively low
values, less than 1.6, for variance inflation factor in the
model run. Heteroskedasticity was inspected in
graphs, and judged not to be serious.
Oaks in crown classes are presented as proportions
and we tested difference in oak stem sizes (diameter)
between classes with permutation test (Lew 2014). To
examine if the oaks were associated with certain tree
species, we tested whether the Betula, Sorbus, Fagus,
and Quercus growing near focal oaks differed from a
random distribution of these trees in the plot (Chi
square test, with expected values based on all stems
C8 m in the plot).
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Results
Stand composition, living trees
In the windthrow, 26 trees remained standing after the
storm: 16 Quercus, two Betula, two Sorbus, two
Fagus, two Picea, one A. glutinosa, and one S. caprea
L. The only large trees in 1969 and 2011 were the 16
Quercus (mean ± SD 51 ± 14.2 cm dbh in 2011) and
the single Salix (49 cm dbh in 2011). All these trees
are excluded below, unless otherwise indicated.
In the study plot, we recorded 2264 stems, 1.3 m
and taller (and three small Picea below 1.3 m). The
stem density per hectare, from highest to lowest, was
as follows: Fagus 672, Sorbus 489, Betula 335,
Corylus 138, Quercus 48, Picea 17, and Salix caprea
5 (in total, 1,704 stems/ha). Within-plot variation in
stem density based on subplots and C.V. was highest
for Corylus (1.15) and decreased as follows for the
other species: Quercus 1.03, Betula 0.46, Sorbus 0.43,
and Fagus 0.33. Thus, Fagus was most evenly
distributed, while Corylus and Quercus occurred more
clumped.
The stem diameter distributions (Fig. 2a) show that
Fagus dominated among smaller trees, though it also
occurred among large (canopy) trees. Sorbus had
intermediate position (also variation in stem sizes)
while Betula had the largest diameters (mean: 22 cm
dbh, maximum 43 cm), and lower variability
(Fig. 2a). The mean size of Quercus stems was
18 cm dbh. The 95 % confidence intervals for mean
stem diameters of the four major tree species were well
separated and did not overlap (Table 2).
The height distributions (Fig. 2b) show that most
Fagus was less than 10 m tall, Sorbus mainly
10–19 m, Betula mainly 15–25 m, and Quercus
mainly 10–24 m tall. The 95 % confidence intervals
for mean height of the species were well separated and
did not overlap (Table 2). Even though Quercus was
on average much taller than Fagus, the large number
of Fagus stems meant that in absolute numbers there
were more Fagus than Quercus that were taller than
15 m (120 vs. 43 trees, respectively).
The standing volume of live trees per hectare in
2011 was highest for Betula (133 m3/ha), and
decreased as follows for the other species: Fagus 73,
Sorbus 49, Quercus 13.4, Picea 4.7, and S. caprea
2.0 m3/ha. If the 16 Quercus trees that survived the
storm in 1969 are included, the figure for this species
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Plant Ecol (2014) 215:1067–1080
would be 27.6 m3/ha. Assuming that roughly half of
this was produced after 1969, we arrive at a figure of
20.5 m3/ha for Quercus, and for all species pooled, the
stand produced 290 m3/ha of live trees up to 2011 (at
least 300 m3/ha if Corylus is included).
The dendrochronological analysis of large trees
within the site showed that stems of Betula established
and grew above breast height over a 20-year period
after the windstorm in 1969 (Table 3). Three of five
Fagus (one outside plot) were older than 40 years, and
two younger. Four of the seven cored Quercus were
established during 1900–1950, and three after 1969.
Finally, two live Sorbus established or grew taller in
the 1970s, and two dead Sorbus stems had reached an
age of about 32 years.
Dead trees, dead wood, and mortality
Based on the 20 subplots, we estimated the dead wood
volume to 32.7 m3/ha. Of this, 68 % was dead trees of
Sorbus (22.4 m3/ha); dead volumes of the other
species, in decreasing order, were Betula 4.7, Quercus
3.2, S. caprea 0.6, and Fagus 0.2 m3/ha. With respect
to diameter of dead stems, Sorbus produced mainly
fine dead wood, Quercus, and Betula mostly coarse
dead wood, and Fagus almost no dead wood (Fig. 3).
Based on summed volume (live plus dead) in the
species, Sorbus produced the highest proportion of
dead wood in relation to its volume (28.4 %) during
the 40 years. Only Corylus had a higher proportion (at
least 50 %; visually estimated). The corresponding
values for the other tree species, in decreasing order,
were: S. caprea 26 % (assuming half of the old tree
from before 1969 was produced after 1969), Quercus
11 %, Betula 6 %, and Fagus 0.3 %. Most dead stems/
pieces from trees were still hard; 96 % of Betula, 90 %
of Sorbus, 90 % of Fagus, and 88 % of Quercus.
Factors influencing tree species composition,
mortality, and regeneration
The tree species composition (in % of total basal area)
was markedly different outside versus within the plot,
with a much higher proportion of Quercus outside
(Fig. 4). Also A. glutinosa, Picea, and Corylus were
more frequent outside the plot, and three tree species
were only recorded outside the plot (Malus sp.,
Fraxinus excelsior L., P. tremula; Fig. 4). In contrast,
Betula, Fagus, and Sorbus were much more common
Plant Ecol (2014) 215:1067–1080
450
(a)
400
350
Number of stems/trees
Fig. 2 a Frequency
distributions of stem
diameter (breast height) for
F. sylvatica, S. aucuparia,
B. pubescens/B. pendula,
and Q. robur/Q. petraea in
the plot. b Frequency
distributions of tree height
for F. sylvatica, S.
aucuparia, B. pubescens/B.
pendula, and Q. robur/Q.
petraea in the plot
1073
Fagus
300
Sorbus
Betula
250
Quercus
200
150
100
50
0
1-4.9
5-9.9
10-14.9
15-19.9
20-24.9
25-29.9
30-35
>35
Diameter (cm) at breast height
600
(b)
Number of stems/trees
500
Fagus
Sorbus
Betula
Quercus
400
300
200
100
0
1-
5-
10-
15-
20-
25-
Height above ground (m)
within the plot. The differences outside versus within
the plot for Quercus, Betula, Fagus, and Sorbus were
marked (Fig. 4), and statistical analysis was judged
unnecessary.
For dead wood of Sorbus, the regression model
included only living volume of Sorbus as significant
predictor (P = 0.001, R2 = 0.49), while living volume of Betula (partial correlation 0.27, P = 0.27) and
Fagus (partial correlation 0.24, P = 0.32) did not
enter into the model. Figure 5 shows the relationship
between dead and living Sorbus in subplots.
In Quercus crown classes (n = 54 trees), no focal
oak was classified as dominant (only old trees
surviving the storm were dominant) and 74 % of the
oaks were co-dominant. All remaining oaks were
intermediates (26 %), and none was overtopped. The
intermediate oaks grew in minor openings among
Betula co-dominants. As expected, co-dominant oak
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Plant Ecol (2014) 215:1067–1080
Table 2 Mean value and confidence interval for stem diameters at breast height (1.3 m) and tree heights (m), for the four
dominating tree species in study plot at Labbra Park Wood, SW
Sweden
Species
Mean
SD
95 % confidence
interval
n (sample
size)
Stem diameter (cm)
Fagusa
Sorbusb
9.1
12.6
6.9
5.8
8.6–9.5
12.2–13.1
890
639
Betulac
22.2
7.1
21.5–22.8
451
Quercusd
17.8
7.1
16.1–19.6
64
Tree height (m)
a
Fagus
8.6
5.1
8.2–8.9
890
Sorbus
12.9
4.6
12.5–13.2
639
Betula
21.1
3.7
20.8–21.5
451
Quercus
15.9
3.9
15.0–16.9
64
Fagus sylvatica
b
Sorbus aucuparia
c
Betula pubescens/B. pendula (pooled)
d
Quercus robur/Q. petraea (pooled)
stems had larger diameter than intermediate oak stems
(mean ± SD
18.8 ± 5.1
vs.
12.5 ± 2.9 cm,
P \ 0.001, permutation test).
In the analysis of trees growing close to focal oaks,
Betula was under-represented compared to a random
distribution of stems, Sorbus and Fagus did not
deviate from random, and Quercus was over-represented (Table 4, P \ 0.001, Chi square test). Oaks
classified as intermediate with respect to crown
(smaller oaks) more often grew near Betula (in
33.3 % of cases) than did co-dominant oaks
(15.8 %), while co-dominant oaks more often grew
close to Sorbus (in 38.3 % of cases) than did
intermediate oaks (19.0 %; 0.025 \ P \ 0.05, Chi
square test). Thus, oaks often grew near other oaks and
less often (than expected) near Betula; and small oaks
often grew near Betula, while larger oaks often grew
near Sorbus.
Discussion
Tree species, succession, and oak regeneration
The cleared windthrow and 40 years of non-intervention produced a tall closed-canopy broadleaved forest.
Quercus was not eliminated, but occurred as 16 large
123
residual trees after the storm and as new trees with
good height growth, but in low density. Ground
disturbances due to storm and logging were probably
important for early establishment of the shade-intolerant Betula (cf. Atkinson 1992). Fewer Betula than
Quercus surrounded the plot, but a Betula tree
produces more seeds and mast years in Quercus only
occur at intervals of about 4–8 years. Up-rooting was
common among the windthrown Picea, and Betula
(and Sorbus) seeds can survive several or many years
in soil (Granström 1987; Raspé et al. 2000). Some of
these may have germinated after soil disturbance, but
new seeds presumably were more important. In a
cleared German windthrow studied during 25 years,
the density of Betula stems [1 m tall continued to
increase over 15 years (Fischer and Fischer 2012),
which is consistent with our dendrochronological
dating of Betula. The under-representation of oaks
near large Betula may be due its fast growth, which
could disfavor Quercus.
Picea forests often contain a relatively shadetolerant ‘‘seedling bank’’ of Sorbus, up to about one
meter tall (Zerbe 2001; Zywiec and Holeksa 2012).
The group of large Picea outside the plot (Fig. 1)
contained such Sorbus in 2011 (pers. obs.) and it is
likely that they also occurred in the windthrow. Many
birds eat the pomes of Sorbus and spread seeds to
conifer stands, good roosting sites (Raspé et al. 2000;
Zywiec and Ledwon 2008). Also, some clonal reproduction occurs in Sorbus, by root suckers (Zerbe 2001;
Zywiec and Holeksa 2012). The windthrown Picea
stand studied by Zerbe (2001) resembled our stand, as
the two major canopy trees were Betula and Sorbus;
Betula was tallest, forming 5 % of the tree cover (total
tree cover 20–50 %). In this study, 80 % of the Sorbus
stems in the windthrow were clonal.
If our windthrow contained many small Sorbus, this
species would have some advantage in the early
succession, explaining its high stem numbers relative
to Betula. In the regeneration 6–7 years after windthrow in Estonia (Vodde et al. 2010), the annual height
growth was highest in Sorbus among the seedlings,
and 36 % higher than in Betula. Later on, Betula
would grow taller and exceed Sorbus in height (this
study, Zerbe 2001). Sorbus is often browsed by
ungulates (Wam and Hjeljord 2010; Zywiec and
Holeksa 2012), but is sometimes relatively resistent
against browsing (Miller et al. 1982; Hester et al.
2004). Hare, roe deer, and moose occurred in
Plant Ecol (2014) 215:1067–1080
1075
Table 3 Cored trees at Labbra Park Wood, SW Sweden, sorted by year of pith
Subplot/site
Species
Diameter (cm)
Height (m)
Year of pith
Establishment, or
diameter in 1969
N6
Betula
18
23
1970
After storm?
N8
Betula
38
23
1970
After storm?
S9
Betula
28
23
1972
After storm
N5
Betula
36
24
1980
After storm
N2
Betula
20
19
1986
After storm
N2
Betula
20
19
1989
After storm
E of plot
a
Fagus
55
23
1940
25
N7
Fagus
62
23
1953
36
N4
Fagus
59
21
1964
16
Near S1
Fagus
?
21
1970
After storm?
S1
Fagus
24
21
1980
After storm
a
NE of plot
Picea
76
?
1925
56
NE of plota
Picea
76
?
1932
48
N3
Quercus
56
26
1900
28
N3
N3
Quercus
Quercus
38
38
24
24
1920
1920
14
14
W of plota
Quercus
32
?
1950
10
N6
Quercus
30
22
1973
After storm
S1
Quercus
16
16
1976
After storm
S2
Quercus
20
18
1977
After storm
N1
Sorbus
20
15
1976
After storm
N6
Sorbus
16
16
1979
After storm
N3
Sorbus
14
18
(32 yr old)
(Dead stem)
N3
Sorbus
14
(piece)
(32 yr old)
(Dead stem)
The trees were cored 50–130 cm above the ground, between 4 April and 24 May, 2011
Species: Betula, B. pubescens/B. pendula; Fagus, F. sylvatica; Picea, P. abies; Quercus, Q. robur/Q. petraea; Sorbus, S. aucuparia
a
Trees growing outside the 1.32 ha study plot
intermediate densities in the plot and browsed sprouts
and small trees during the early succession stages.
Sapling density in the stand was then very high
(T. Appelqvist, pers. comm.) which may have diluted
the per capita (per stem) impact on trees by ungulates,
assuming territorial behavior (Vivås and Saether
1987). It is also possible that Sorbus and Quercus
densities would have been higher without hare and
ungulates in the forest. The current browsing pressure
from ungulates in southern Sweden is higher than
during the mid-late 1970s and have led to damages on
saplings of oak in several forest types (Götmark et al.
2005; Bergquist et al. 2009). However, there are few
studies of broadleaved-dominated young stands. One
Betula-dominated stand (former Picea stand, clear-cut
in 1999), 15 km from Labbra Park Wood, had
produced 84 oak saplings per hectare up to 2013,
despite higher density of ungulates than during the
1970s (Götmark 2014, on-going study).
Almost all Fagus were alive: saplings, and dominant trees that resembled the other trees (straight
stems, small crowns). Large wide beeches grew quite
far away from the plot in 1969 (Fig. 1), but coring
revealed two smaller beeches in the plot before the
storm. They may explain part of the abundant beech
regeneration. Rodents (Perea et al. 2012), jays (Garrulus glandarius L., Nilsson 1985), and other animals
disperse acorns and beech nuts, and high shade
tolerance (Packham et al. 2012) favored Fagus in the
understory.
123
1076
Plant Ecol (2014) 215:1067–1080
60
250
50
Dea
ad Sorbus (cubic m/ha)
Number of pieces/stems
300
Fagus
200
Sorbus
Betula
150
Quercus
100
50
40
30
20
10
0
5-
10-
15-
20-
25-
30-
35-
40-
Dead wood diameter (cm)
0
0
Fig. 3 Distribution of dead wood in diameter classes (stems
and stem pieces) for F. sylvatica, S. aucuparia, B. pubescens/B.
pendula, and Q. robur/Q. petraea in the plot
20
40
60
80
100
120
140
Live Sorbus (cubic m/ha)
Fig. 5 The positive relationship between the volumes of dead
and live wood of S. aucuparia in the 20 subplots
Proportion (%) of total basal area
70
Table 4 The distribution of trees (stems taller than 8 m) near
focal oaks, compared to expected values under random distribution of stems
60
50
Species
Basal area outside
40
30
20
10
us
s
ul
Po
p
us
nu
xi
Fr
a
li x
al
M
Sa
us
s
us
rb
So
yl
Co
r
us
nu
Pi
Fa
g
s
a
ce
Pi
la
nu
tu
Al
us
rc
Be
ue
Expected nob
Fagus sylvatica
43
Sorbus aucuparia
54
58.6
Betulac
33
51.4
Quercusd
30
9.0
160
160
Total
0
Q
Number of stems
Recorded noa
Basal area in plot
a
41.0
Three stems, the closest ones, recorded for each focal oak
b
Fig. 4 Comparison of tree basal area (breast height) proportions between plot and forest surrounding the windthrow (for
further explanation, see ‘‘Methods’’ section). Species as in
Figs. 2, 3, and in this figure, and A. glutinosa, P. abies, P.
sylvestris, C. avellena, S. caprea, Malus sp., F. excelsior, and P.
tremula
We found few trees of the shade-tolerant Picea,
despite several mature Picea in the plot and the tree
group east of the plot. Similar results were reported by
Zerbe (2001), despite the many large spruces growing
next to his windthrow. Picea do not survive in a soil
seed bank (e.g., Alvarez et al. 2012) and seem to
require canopy openings (Drobyshev and Nihlgård
2000; Jonasova et al. 2006). We suggest that the dense
stand of Betula, Sorbus, and Fagus was too dark for
Picea colonization or Picea survival.
123
Expected numbers calculated for Chi square test; all
recorded stems in whole plot were first summed, and species
proportions from this total number used to obtain expected
values for the sample of trees (n = 160) growing close to focal
oaks (P \ 0.001)
c
Betula pubescens/B. pendula, pooled
d
Quercus robur/Q. petraea, pooled
Our prediction that Betula and Fagus should
compete with and disfavor Sorbus was not supported;
instead, the self-thinning alternative was supported.
Some other studies have found similar self-thinning in
mixed forests (e.g., Stoll and Newbery 2005). Most
dead Sorbus had not reached large size, had small
crowns, no obvious signs of insect or fungal attack,
and the dead wood was hard. If some Sorbus consisted
of clones (genets), self-thinning of stems (rami) within
genets may help explain our results. Rami in poor
Plant Ecol (2014) 215:1067–1080
condition and in poor light below the canopy (grownup Sorbus have high light demands; Raspé et al. 2000;
Zerbe 2001) may have been shed, to favor other parts
of the genet. Although canopy shading by Betula,
Fagus, and Quercus may have contributed to some of
the mortality in Sorbus (von Oheimb et al. 2011), our
results suggest that self-thinning was a major factor.
Our study shows that after a strong disturbance
Quercus was not eliminated during long-term competition and succession. The new large oaks were
spatially clumped, both in the analysis of subplots
and of focal oaks (stem level). Oak seedlings colonizing forest plots in south-central Sweden that lacked
adult oaks were also clumped in space (Frost and
Rydin 2000). A clumped pattern of large oaks may be
due to (1) jays (that nest in the area) hoarding acorns in
scattered semi-open patches (Bossema 1979), where
oaks may survive better; (2) rodents that hoard in
caches; and (3) differential survival of seedlings/
saplings/trees during succession, and in relation to
light (Götmark 2007). The focal oaks were underrepresented and smaller near Betula, possibly due to
competition, and larger focal oaks were more common
near Sorbus. Mortality was clearly higher for Sorbus,
which in turn may have favored growth and reduced
the mortality of medium-sized and large oaks.
Comparison with other similar studies, and key
traits for persistence in Quercus robur/Q. petraea
We found eight other studies of windthrow with
salvage logging, or clear-cutting for stand conversion
to broadleaved trees, with no other treatment than
initial harvest. To include a study for comparisons, we
required that Q. robur/Q. petraea occurred near the
site or in the landscape nearby. The studies were sorted
into three groups: (1) age of the created and studied
opening 1–10 years (Dobrowolska 2006; Jonasova
et al. 2006; Karlsson and Nilsson 2005); (2) age of
opening 14-19 years (Zerbe 2001; Harmer and Morgan 2009; Götmark 2014); and (3) age of opening
39–40 years (Peterken and Jones 1989, Kelly 2002).
Overall, these studies indicate persistence of Q. robur/
Q. petraea at low density in the new stands, when
these taxa occur in the surroundings at the time of
disturbance. The three studies of the youngest clearings involved former coniferous stands, which after
clearing differed in regeneration of oak seedlings
(44–95,000 per ha) and saplings (16–1,537 per ha),
1077
and high regeneration was related to high density of
mature oaks in the surroundings of the clearings. The
three studies of openings 14–19 years reported relatively high sapling/tree densities in two cases (84–400
saplings per ha) and low densities in one case (see
Harmer and Morgan 2009). The Irish stand in the third
group (opening 39–40 years) had relatively high oak
density (338 saplings and 78 trees per ha), but the site
was small with few oaks, with crowns below the
Betula canopy (Kelly, pers. comm.). Finally, the
studies of Lady Park Wood (Peterken and Jones 1989)
and Labbra Park Wood ended up with similar densities
of oak trees after 40 years of succession (28 and 48
oaks per ha, respectively).
For re-colonization of Quercus after stand-replacing disturbances, its occurrence in nearby is important.
Our study and the literature indicate capacity for Q.
robur/Q. petraea to colonize after disturbances, and
persistence up to 40 years. More long-term studies of
Quercus are needed. In North America, a study of
regrowth in 21–35 year old clear-cuts indicated that
Quercus stump sprouts, among other factors, contributed to oak competitive success (Morrissey et al. 2008,
see also Johnson et al. 2009). For Quercus spp. in
floodplains in the US, growth rates were as good as for
other tree species in fully cleared areas, but not under
partial shade (Oliver et al. 2005). In a forty year study
(1938–1978) of regeneration after windthrow in New
England, Q. rubra L. and Betula papyrifera Marshall
became dominants in the canopy (Hibbs 1983).
One can argue that the density of oaks in our plot
was low compared to that of the other tree species, and
that strong regeneration of Fagus suggests that this
species excludes Quercus in the future (see, for
instance, Leuschner et al. 2001; Schnitzler and Closset
2003; Rohner et al. 2012). In the plot, Fagus was the
only tree species that had many saplings in the
understory (in good condition) and the future stand
may become strongly dominated by Fagus, unless this
species is disfavored by e.g., disease. This raises the
question how Q. robur/Q. petraea persist in relatively
natural, temperate European forests with several
shade-tolerant tree species.
Lindbladh and Foster (2010) and others documented very long-term, relatively stable persistence of
Q. robur/Q. petraea in forests over a large part of the
Holocene. We suggest three key traits that should
contribute to make the taxa successful: (1) long life
span, (2) ecological plasticity, and (3) resistance to
123
1078
disturbances. Firstly, Q. robur/Q. petraea can reach an
age of at least 920 years (Lindquist 1939) which
increases the chance of reproduction under unfavorable conditions that may last long. Secondly, Quercus
has a broad niche (Lawesson and Oksanen 2002,
p. 284); is plastic in growth form, with wide canopies
in open-grown trees, and tall straight stems in dense
stands (Jones 1959, present study); adapt to disturbances and openness by sprouting from stems and
stumps (Jones 1959); can grow as fast as pioneer trees
(Peterken and Jones 1989, present study) but in
contrast to these trees survive as seedling/sapling in
relatively dark understories; and can reproduce
early—at 5 cm dbh (F.G., pers. obs.) or from an age
of 15(-25) years (Jones 1959). Thirdly, as we show,
Quercus survives severe storms standing, and the trees
are probably relatively resistant against wildfire
(Bradshaw and Hannon 2004; Proenca et al. 2010)
and flooding (Dobrowolska 2007; Kramer et al. 2008).
Conclusions and implications
Tall shade-intolerant Betula and Sorbus, and shadetolerant Fagus, dominated the windthrow 40 years
after it had been cleared. Old and new trees of midtolerant Q. robur/Q. petraea (Niinemets and Valladares 2006) was another component; at low density, but
their long-term persistence in this forest is clear. A
similar result was reported by Peterken and Jones
(1989), from a forest which is still studied (Peterken,
pers. comm.). Extensive self-thinning of Sorbus
occurred and occurs, and in the future possibly strong
dominance of Fagus. Three life-history traits help in
explaining the long-term success and persistence of Q.
robur/Q. petraea in European forests: long life span;
ecological plasticity in habitat and growth; and
resistance against severe disturbances. Finally, salvage logging is debated (Lindenmayer et al. 2008) but
there are few long-term studies; here we show that a
species-rich and timber-rich forest can be produced
under non-intervention following salvage logging.
Such stands may be useful for conservation (Götmark
2013), silviculture (see list of References), and
research.
Acknowledgments We thank Ralph Harmer, Igor Drobyshev,
Anna Monrad Jensen, associate editor, and anonymous
reviewers for valuable comments on the manuscript. Daniel
123
Plant Ecol (2014) 215:1067–1080
Kelly kindly provided unpublished data; Ralph Harmer also
kindly provided additional information. Mats Niklasson and
Igor Drobyshev helped us with dendrochronology. The stand
and nature reserve was studied under permission from the
Härryda municipality. The municipality also provided the aerial
photograph of the forest, and helped us in studies of archives.
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