Stand structure and plant species diversity in managed and

Forest Ecology and Management 270 (2012) 232–238
Contents lists available at SciVerse ScienceDirect
Forest Ecology and Management
journal homepage: www.elsevier.com/locate/foreco
Stand structure and plant species diversity in managed and abandoned silver
fir mature woodlands
T. Sitzia a,⇑, G. Trentanovi a, M. Dainese a, G. Gobbo b, E. Lingua a, M. Sommacal b
a
b
Università degli Studi di Padova, Dipartimento Territorio e Sistemi Agro-forestali, Viale dell’Università 16, I-35020 Legnaro (PD), Italy
Italian Ministry of Agricultural, Food and Forestry Policies, State Forestry Corps, Ufficio Territoriale per la Biodiversità, Via Gregorio XVI 8, I-32100 Belluno, Italy
a r t i c l e
i n f o
Article history:
Received 15 December 2011
Received in revised form 17 January 2012
Accepted 19 January 2012
Keywords:
Woodland conservation
Unmanaged forests
Stand diversity
Mixed models
Vascular species
Deadwood
a b s t r a c t
Although few undisturbed forests remain in Europe, forest reserves and deforested areas that are no
longer profitable have the potential to develop stand structures similar to those which preceded human
disturbances. The direct effects of management cessation on forest diversity are confounded by many factors that should be controlled when comparing managed and abandoned stands. In the European Alps,
however, the high variability of habitats makes it nearly impossible to find comparable stands located
within forests large enough to be independent from the surrounding land. The aim of this study was
to investigate the use of mixed models to compare deadwood and plant diversity between matched managed and unmanaged pairs of forests, with the hypothesis that their differences were due to direct effect
of abandonment. Two neighbouring watersheds that were large enough to be independent from the surrounding forests were chosen. These watersheds had a common history of use, but one was non-intensively managed, while the other was untouched since 1957. Ten plots were randomly selected from
each forest. Mixed models confirmed their matched topography and stand structure, while a similarity
index confirmed their assignment to the same plant community. The unmanaged stand had higher soil
nitrogen, higher Fagus sylvatica dendrological composition, higher tree species richness, higher dead logs
and a different composition of the tree and understory layers. These results suggest that silver fir woodlands abandoned for more than 50 years change spontaneously and that this approach may be an effective means for studying other forest communities.
Ó 2012 Elsevier B.V. All rights reserved.
1. Introduction
Millennia of human activities have left Europe with only 1% of
its landmass covered with relatively natural woodlands (Heywood
and Watson, 1995; Vanbergen et al., 2005); in Italy natural woodlands cover only 0.032% of the forested surface (Maesano et al.,
2010; Marchetti et al., 2010). However, woodlands inside strict forest reserves (MCPFE, 1998; Parviainen et al., 2000) have the potential to develop towards old-growth forests (Gilg, 2004) that have
stand structures and features similar to those which preceded human disturbances (Schnitzler and Borleab, 1998; Parviainen et al.,
2000; Motta et al., 2010). In addition because silviculture is often
abandoned when unprofitable, such as in the Alpine and in the
Mediterranean regions (Piussi, 1991; Fabbio et al., 2003; Pettenella
and Secco, 2006), the area of unmanaged woodlands is expected to
increase in the future.
The dynamics and functional processes that follow forest abandonment are occurring in an increasing portion of European forests. In general, past silvicultural treatments have influenced tree
⇑ Corresponding author. Tel.: +39 0498272747; fax: +39 0498272686.
E-mail address: [email protected] (T. Sitzia).
0378-1127/$ - see front matter Ó 2012 Elsevier B.V. All rights reserved.
doi:10.1016/j.foreco.2012.01.032
composition, growing stock, stand vertical structure and deadwood
(Boncina, 2000; Christensen et al., 2005; Debeljak, 2006), as well as
biotic components other than trees (see Harmon et al., 1986; Carey
and Johnson, 1995; McAlister, 1995; Gunn and Hagan, 2000; Gibb
et al., 2006). Consequently, the effects of abandonment may have
few practical implications in the short-term, but relatively greater
significance in the long-term (White and Mladenoff, 1994; Ruffner
and Abrams, 1998; Motta and Garbarino, 2003; Paillet et al., 2010).
There is an extensive literature on biodiversity differences between managed and unmanaged European forests. However, little
has been reported with a sampling design that can match landscape conditions, plant communities and stand development stage,
which could override the effects of abandonment. Due to the high
variability of the forests in the Alps, it is particularly difficult to
control these confounding factors on large samples of forests. In
addition, unmanaged samples should be located within large enough areas so that they are not influenced by the neighbouring
managed forests (see Paillet et al., 2010 for a review).
For above mentioned reasons, comparative studies between
managed and unmanaged forests in the Alpine environment are
rare (but see Boncina, 2000; Motta et al., 2008), and a feasible
approach is to compare just two stands (Burrascano et al., 2008)
T. Sitzia et al. / Forest Ecology and Management 270 (2012) 232–238
located not far from each other and similar in their characteristics.
Providing that the unmanaged one is part of a forest large enough
not to be influenced by the neighbouring managed forests and that
it was subject to past logging of similar intensity, the other variables to be matched should be firstly chosen among those relatively
independent of management, like plant community and topography. Then, since stand structure is closely related to functions, in
terms of biodiversity and soil quality, controlling the former implies
that the specific relationships between stand structure and functions would vary according solely to the effect of disturbance regimes (Fujimori, 2001). Therefore, when stand structure matches,
a further level of control is permitted. In contrast, the partial contributions of the main tree species to tree density, basal area, volume
and crown cover are stand measurements, collectively called dendrological composition (Hellrigl, 1986), that are related to the periodic effect of intermediate cuttings and should be encountered as
variables dependent on abandonment of management.
Even after having taken these precautions, observations from
the same geographical area may be correlated either in space or
through time. Therefore, examining the effects of abandonment
would be still confounded by the difficulty of separating the effects
of abandonment from spatial or temporal pseudo-replicated correlations between and within forest samples (Hurlbert, 1984). Because mixed models have shown great potential for avoiding the
problems of pseudo-replication in other ecological fields (Paterson
and Lello, 2003; Millar and Anderson, 2004), their efficacy in
detecting differences between matched pairs of managed and
unmanaged forests under varying site conditions would be of considerable interest.
In this study, mixed models were used to compare soil quality,
dendrological composition and three groups of biodiversity variables (deadwood and vascular species richness and composition)
within two silver fir (Abies alba) woodlands of the Alps that were
matched for topography, stand structure and plant community.
Differences will be discussed hypothesising their relation to the
abandonment of management.
2. Material and methods
2.1. Study areas
The study was carried out in an Alpine forest district of northeastern Italy. The mean annual temperature is 7.2 °C and mean annual precipitation is 1300–1500 mm year1; precipitation is mainly
concentrated in May–June and October–November. The most common forest soils are Cambisols, and the substrate is limestone
deposits.
Two neighbouring 1040 ha watersheds (Tovanella and Cajada)
were selected for this study (Fig. 1). The two watersheds are at
the same altitudinal range (550–2500 m a.s.l.) and are currently
subjected to contrasting forest management regimes, but have a
common past-history of use. During 1943–1953, these forests were
heavily exploited (up to 150% ratio of yield to increment), which
reduced them to very low growing stock (<200 m3 ha1) with a
paucity of good quality and large trees (Susmel, 1958).
Silviculture and grazing were stopped in the forests of the Tovanella watershed (46°180 N, 12°180 E) in 1957 (Susmel, 1958) and
have been part of a nature reserve since 1971 (Viola et al., 2008).
The forests of the Cajada watershed (46°140 N, 12°140 E) are currently non-intensively managed for timber production using group
selection logging based on a 12-year cutting cycle with exploited
areas <1000 m2. The mean annual harvest is 1.72 m3 ha1, corresponding to 0.65% of the growing stock and 33.2% of the annual
increment (Andrich, 2005). This research focused on the silver fir
woodland type, which is widespread in the mountainous regions
233
of Europe (Liu, 1971) and is one of the most valuable for timber
production (Mayer, 1979; Sagnard et al., 2002; Gabrielli, 2003)
and biodiversity conservation (Becker, 1989; Senn and Suter,
2003; Gärtner and Reif, 2004; Heuze et al., 2005; Bottacci, 2009).
According to Ozenda (1985) the silver fir woodlands studied here
lie within the inner mountain belt of the southern calcareous
pre-Alps and belong to the inner vegetation series of A. alba.
2.2. Data collection
Ten sample units were randomly selected on slopes lower than
26° within stands that appeared mature and were mapped by Lasen et al. (2008) and Andrich (2005) as calcareous silver fir woodlands. Each sample unit was a circular 12.5 m radius plot with a
6 m sub-plot and two transects.
In each circular plot, all trees (DBH > 7.5 cm) were mapped and
the following parameters were recorded: DBH, species, total
height, height of crown insertion and four vertical crown projection radii. The resulting stand structure attributes were consistent
with a mature stage (Susmel, 1981). Natural regeneration was
sampled, but was negligible, as expected for a mature stage.
The amount of Coarse Woody Debris (CWD) was obtained by
differently sampling the diverse deadwood elements (Motta
et al., 2006; Castagneri et al., 2010). To assess number and volume
of logs (larger diameter P10 cm), Line Intersect Method (Van
Wagner, 1982; Marshall et al., 2000) was used, while for stumps
(dead trees height <1.30 m and diameter at 50 cm-height
P10 cm) and snags (height P1.30 m and diameter at 50 cm-height
P10 cm), two 50 8 m rectangular transects spreading from the
plot centre towards the north and east were used.
Diameter (stem, base and top for stumps or two extremes for
logs), height and decay classes were measured on each of the dead
features. The decay stages of logs and snags were classified according to a five class system (Maser et al., 1979; Sollins, 1982). The decay stage of stumps was classified according to a four class system
(Motta et al., 2006). For each understory vascular species, we estimated the Braun-Blanquet (1932) index of cover with surveys conducted within the 12.5 m-radius plot.
On the same two transects used for the CWD, the plant species
intersecting every 1 m segment was recorded. Ellenberg indicator
values for moisture, nitrogen and soil reaction (Ellenberg et al.,
1991) were used to evaluate soil quality. Community-level
weighted means (Lavorel et al., 2008) of Ellenberg indicator values
were calculated for every transect using frequency data in species
composition.
2.3. Assessment of matched conditions
The assignment of the understory relevés to the same Adenostylo glabrae–Abietetum albae vegetation unit of a regional phytosociological classification (Del Favero and Lasen, 1993) was verified
using the Frequency-Positive Fidelity Index (FPFI) (Tichý, 2005).
Linear mixed models with a restricted maximum likelihood (REML)
estimation procedure were applied to verify the matched conditions of stand structure, where forest management was a fixed factor (managed vs. abandoned) and plot was a random factor. Stand
structure variables included the following: tree diameter (TDD)
and height (THD) diversity (see Kuuluvainen et al., 1996), the mean
DBH and mean tree height across all species and of the three dominant tree species individually, total volume and total basal area of
living trees.
2.4. Assessment of abandonment effects
While stand structure was controlled to allow a comparison
between the two forests, the effects of abandonment on
234
T. Sitzia et al. / Forest Ecology and Management 270 (2012) 232–238
Fig. 1. Italy, Veneto Region and location of the surveyed watersheds (triangle: Cajada, star: Tovanella).
dendrological composition (in terms of their tree density, basal
area, volume and crown cover) of the three dominant tree species,
as well as soil quality, tree and understory species richness and
CWD, were also examined with the same mixed models. Crown
cover values were angular transformed prior to analysis (Zar,
1999).
Non-metric multi-dimensional scaling (MDS) ordination based
on the Bray–Curtis similarity index and Permutational Multivariate
Analysis of Variance (PERMANOVA) (Anderson, 2001) were used to
test for differences in tree and understory composition among the
managed vs. abandoned stands. Forest management was a fixed
factor. Upon finding a significant PERMANOVA, a Permutational
Analysis of Multivariate Dispersions (PERMDISP) (Anderson et al.,
2006) was employed to discern whether the compositional differences were within or between the two forests. To test the response
of tree and understory species composition to forest management,
Indicator Species Analysis (ISA) (Dufrêne and Legendre, 1997) was
used. These species were identified for each forest cluster with the
indicator value (IndVal) method, which combines the specificity of
a species (its uniqueness to a particular forest management) and its
fidelity (its frequency within that forest management). For each
species, the IndVal ranges from 0 (no indication) to 1 (maximum
indication). Statistical significance of IndVal was tested by means
of a Monte Carlo test, based on 999 randomisations.
All statistical analyses were performed using the following R
software (R Development Core Team, 2009) packages. Linear mixed
models were performed using ‘nlme’ package (Pinheiro et al.,
2010). The functions ‘adonis’ and ‘betadisper’ in the package ‘vegan’ (Oksanen et al., 2011) were used to compute PERMANOVA
and PERMDISP (999 permutations), respectively. Non-metric multi-dimensional scaling (MDS) ordination was performed using ‘labdsv’ package (Roberts, 2010). The Indicator Species Analysis was
performed using the ‘indicspecies’ package (De Caceres and
Legendre, 2009).
Table 1
Mean ± SD of topographic and stand structural attributes of the two types of
woodlands (managed and abandoned). P values were obtained by linear mixed
models with a restricted maximum likelihood (REML) estimation procedure (forest
management was a fixed factor, while plot was a random factor).
Variables
Managed
Abandoned
F value
P level
Topography
Altitude (m a.s.l.)
Slope (°)
1228 ± 43
16.1 ± 5.4
1221 ± 103
14.8 ± 8.0
0.045
0.182
0.834
0.675
50.5 ± 13.2
663 ± 183
2.0 ± 0.2
1.6 ± 0.3
46.8 ± 10.0
556 ± 154
1.9 ± 0.2
1.7 ± 0.3
0.502
1.979
0.931
0.897
0.488
0.177
0.532
0.428
34.6 ± 17.2
38.1 ± 21.7
15.2 ± 6.8
32.7 ± 17.1
39.8 ± 19.5
14.8 ± 6.5
0.623
0.066
0.062
0.440
0.801
0.807
21.4 ± 9.6
19.4 ± 12.1
12.1 ± 4.6
20.2 ± 9.3
22.0 ± 8.3
14.2 ± 5.1
0.181
0.030
4.180
0.676
0.864
0.057
Stand structure
Basal area (m2 ha1)
Volume (m3 ha1)
TDD
THD
DBH (cm)
Abies alba
Picea abies
Fagus sylvatica
Height (m)
Abies alba
Picea abies
Fagus sylvatica
3. Results
3.1. Matched conditions
Both of the sampled forests were assigned to the A. glabrae–A.
albae (FPFI >85%) forest type. Table 1 shows that neither topographical nor stand structure attributes differed between the managed and the abandoned forest. These results indicate that the two
forests are matched for phytosociological association, site
conditions and stand structure.
235
T. Sitzia et al. / Forest Ecology and Management 270 (2012) 232–238
Table 2
Mean ± SD of tree structural parameters of the two types of woodlands (managed and
abandoned). P values were obtained by linear mixed models with a restricted
maximum likelihood (REML) estimation procedure (forest management was a fixed
factor, while plot was a random factor).
Variables
Abandoned
F value
P level
5.0 ± 0.3
5.0 ± 0.8
4.6 ± 0.7
4.9 ± 0.1
5.0 ± 0.5
5.6 ± 0.4
0.949
1.701
18.143
0.343
0.209
<0.001
273 ± 165
98 ± 81
120 ± 81
200 ± 103
108 ± 52
291 ± 176
1.426
2.969
6.937
0.355
0.227
0.011
Basal area (m2 ha1)
Abies alba
Picea abies
Fagus sylvatica
32.0 ± 14.8
14.7 ± 11.9
2.6 ± 2.1
21.3 ± 9.3
16.6 ± 7.9
6.0 ± 3.9
3.698
0.166
5.656
0.194
0.723
0.032
Volume (m3 ha1)
Abies alba
Picea abies
Fagus sylvatica
442 ± 197
197 ± 162
24 ± 25
278 ± 144
193 ± 89
61 ± 41
4.499
0.004
5.970
0.048
0.954
0.025
Crown cover (%)
Abies alba
Picea abies
Fagus sylvatica
57.8 ± 13.3
20.3 ± 13.8
28.6 ± 19.7
52.3 ± 17.8
34.0 ± 14.0
55.6 ± 13.8
0.613
4.840
12.586
0.516
0.037
0.005
2.9 ± 0.3
38.6 ± 6.9
4.2 ± 0.9
34.4 ± 6.6
17.894
1.930
<0.001
0.182
38.6 ± 9.9
6.0 ± 3.5
14.1 ± 8.5
18.5 ± 10.2
10.736
26.161
18.540
32.394
0.004
<0.001
<0.001
<0.001
Soil quality (Ellenberg values)
Moisture
Reaction
Nitrogen
Dendrological composition
Density (No. trees/ha)
Abies alba
Picea abies
Fagus sylvatica
Species richness (No. species)
Trees
Understory
Managed
Coarse Woody Debris (m3 ha1)
Total CWD
24.8 ± 8.8
Stumps
23.0 ± 9.9
Snags
1.7 ± 3.4
Logs
0.2 ± 0.2
Table 3
PERMANOVA (Permutational Multivariate Analysis of Variance) and PERMDISP
(Permutational Analysis of Multivariate Dispersions) results comparing tree and
understory composition between the two types of woodlands (managed and
abandoned). Comparisons were performed using the permutation test (n = 999).
F value
P level
PERMANOVA
Tree composition
Understory composition
2.980
5.164
0.016
0.001
PERMDISP
Tree composition
Understory composition
0.499
1.702
0.484
0.226
Table 4
Indicator Species Analysis (ISA) of the two types of woodlands (managed and
abandoned) for tree composition. IndVal values were tested using permutation tests
(n = 999). Significant indicator species are presented in bold.
Species
Managed
Abandoned
P level
Tree layer
Abies alba
Acer platanoides
Fagus sylvatica
Laburnum anagyroides
Larix decidua
Picea abies
Salix caprea
Sorbus aucuparia
0.76
0.00
0.51
0.00
0.00
0.69
0.00
0.00
0.65
0.32
0.84
0.32
0.84
0.72
0.32
0.32
0.277
1.000
0.005
1.000
0.004
0.787
1.000
1.000
Understory
Abies alba
Athyrium filix-femina
Circaea alpina
Dryopteris dilatata
Euphorbia dulcis
Fragaria vesca
Helleborus viridis
Hepatica nobilis
Lonicera nigra
Luzula nivea
Maianthemum bifolium
Mercurialis perennis
Phegopteris connectilis
Senecio cacaliaster
Vaccinium myrtillus
0.26
0.71
0.82
0.84
0.00
0.93
0.00
0.80
0.89
0.95
0.92
0.30
0.85
0.89
0.91
0.94
0.00
0.06
0.27
0.71
0.06
0.77
0.20
0.00
0.22
0.34
0.84
0.39
0.00
0.15
0.012
0.030
0.020
0.025
0.025
0.004
0.007
0.024
0.001
0.007
0.032
0.049
0.008
0.003
0.003
3.2. Abandonment effects
Abandonment was related to an increase in soil nitrogen (Table 2). According to Schaffers and Sýkora (2000), this difference
must be due to the lower timber productivity of the abandoned
forest, followed to the cessation of logging and accumulation of
deadwood (Harmon et al., 1986). Furthermore, the cessation of logging, together with chronic N deposition, may have produced an
excess N accumulation relative to C accumulation in soil (Binkley,
1995; Goodale and Aber, 2001).
Table 2 shows that all species differed between the two forests
in at least one of the dendrological parameters. Beech (Fagus sylvatica) differed in all parameters, spruce (Picea abies) differed only in
crown cover and silver fir differed only marginally in volume.
Beech must have increased due to the cessation of coppicing, while
the spontaneous development is likely re-equilibrating silver fir
partial volume to a more mixed natural state, conserving its
Fig. 2. Nonmetric multidimensional scaling (MDS) ordination plots of community composition in two-dimensional space: (a) tree species and (b) understory species. Each
point represents the composition of a community (open circles: managed plots; grey circles: abandoned plots) in multidimensional space and the distance between any two
points represents the difference between those two communities according to a Bray–Curtis dissimilarity metric.
236
T. Sitzia et al. / Forest Ecology and Management 270 (2012) 232–238
Table 5
Decay class distribution (%) of snags, stumps, logs in the two types of woodlands (managed and abandoned). Snags and logs have five decay classes and stumps have four decay
classes.
Decay class
1
2
3
4
5
Snags
Logs
Stumps
Managed
Abandoned
Managed
Abandoned
Managed
Abandoned
75
25
0
0
0
20.8
58.3
14.6
4.2
2.1
17.9
12.8
35.9
30.8
2.6
11.5
15.6
40.6
20.8
11.5
2.7
17.6
42.3
37.4
0
13.7
48.7
37.6
participation to the canopy cover that is becoming saturated by the
other two co-dominant tree species.
The abandoned forest had a higher number of tree species (Table 2), as well as differences in tree species composition (Table 3
and Fig. 2a). As shown in Table 4, these differences were due to
the cessation of beech coppicing and to the presence of seven old
isolated Larix decidua trees (mean diameter: 38 cm), which are pioneer individuals whose development was favoured by the effects of
the heavy past exploitation. In the managed forest, the regular forestry treatments likely caused the removal of these species. There
were no differences in understory species richness (Table 2), supporting the idea that, apart from the time immediately following
heavy thinning, the forest floor is little influenced by management
(Graae and Heskjaer, 1997). However, from Fig. 2b and Table 3, it
can be seen that the two forests differ in their understory composition. Table 4 shows that several indicator species of the Cajada
understory in the managed forest (Fragaria vesca, Senecio cacaliaster and Vaccinium myrtillus) have a preference for higher light levels, whereas indicator species in the abandoned forest are more
shade tolerant (silver fir seedlings, Euphorbia dulcis, Helleborus viridis and Mercurialis perennis). This is consistent with the differences
found in canopy cover (Table 2). The PERMDISP analysis (Table 3)
revealed that the composition of trees and understory were
homogenous within each forest.
The managed forest had a significantly lower volume of total
CWD, snags and logs, but a higher volume of stumps (Table 2).
The latter was likely reduced in the abandoned forest after the cessation of cutting. The fact that logs were more concentrated in the
third and the fourth decay classes in both the forests, while snags
were are almost exclusively concentrated in the first and in the
second decay classes, strongly confirms that logs fall on the ground
after spending the first and second decay stages as a snag; that is,
most trees die when they are standing because of competition
(Motta et al., 2006) (Table 5). Finally, stumps were concentrated
in the two most advanced decay classes. In all, these results are
consistent with those obtained in many previous studies (Fridman
and Walheim, 2000; Debeljak, 2006).
4. Discussion
Many authors have shown that the cessation of management in
similar forest stands, with the same history of use, determines
changes in the dendrological composition of trees in those stands
(e.g. Kuuluvainen et al., 1996; Boncina, 2000; Uotila et al., 2001;
Motta and Garbarino, 2003). Furthermore, deadwood generally increases with abandonment in a wide range of communities (e.g.
Hansen et al., 1991; Kirby et al., 1991; Green and Peterken, 1997;
Marage and Lemperiere, 2005; Lombardi et al., 2008; Castagneri
et al., 2010; Calamini et al., 2011) and may contribute to soil nitrogen content (Harmon et al., 1986). In contrast, prior research has
documented the general uncertainty regarding how abandonment
influences the richness and composition of plant species (Graae
and Heskjaer, 1997; Burrascano et al., 2009; Paillet et al., 2010).
Most of the previous studies have either been conducted in areas
outside of the Alps, such as boreal forested landscapes, or have not
focussed on matched conditions, where the confounding effects of
landscape heterogeneity was controlled. This study examined the
extent to which abandonment, when compared between two
forests where other confounded factors were controlled, improved
soil quality, dendrological composition, vascular species richness
and composition and the amount of deadwood. It was found that
in mature stands of silver fir woodlands, 50 years of abandonment
were associated with substantial increases in soil nitrogen, tree
species richness and log and snag volume. In addition, dendrological and plant community composition significantly and homogenously changed due to an increase of proportion of beech and
shade tolerant understory species. The former is confined to the
intermediate and codominant layers where a large proportion of
silver fir is also present, while the dominant layers consist of old silver fir and spruce trees; thus, the general structure is developing
towards a two-layered forest type. Light needs were higher in the
indicator species of the managed forest and were related to the
lower degree of cover of the tree layer (Schmidt, 2005).
These findings extend those of many previous studies (Boncina,
2000; Motta and Garbarino, 2003; Bianchi and Paci, 2008; Vrska
et al., 2009), confirming that the management of silver fir woodlands has often led to the reduction of beech and other broadleaved
species. This could be because they were frequently cut to produce
firewood for mining purposes or because they were not economically important (Málek, 1981; Johann, 2007) compared to fir and
spruce, as was the case in Cajada and Tovanella (Susmel, 1958; Lazzarini, 2006) and in the neighbouring Trento province (Ferrai and
Mazzucchi, 1981).
This study confirmed the importance of deadwood patterns in
identifying different historical development in similar forest stands
and that, among all deadwood types, logs in different decay and
size classes can be used as an index to evaluate habitat continuity
over recent times (Stokland, 2001).
The changes noted in this study were unrelated to topographical, conditions and stand development. This study therefore indicates that the methodological benefits gained from matched
conditions and sampling, combined with a mixed model analysis,
may address the effect of abandonment across a wide range of forest communities.
5. Conclusions
This study applies a combination of sampling design and analysis in the Alps with two biotic components. The results provide
evidence that silver fir woodlands where logging has been abandoned for more than 50 years are changing spontaneously in their
diversity due to an increase in tree species richness and changes in
herbaceous composition, and they suggest that this approach may
be effective for studying these processes in other kinds of forest
communities as long as they are not strongly influenced by the
neighbouring managed forest.
T. Sitzia et al. / Forest Ecology and Management 270 (2012) 232–238
Some limitations of this study are worth noting. Although the
main hypothesis was supported statistically, sampling should be
extended to other biotic components (e.g. birds, insects, fungi
and lichens) and case studies in order extend these results to the
entire forested landscape of the Alps. Furthermore, as suggested
by Paillet et al. (2010), future work should examine the effect at
multiple time points since abandonment on the same study area
to evaluate whether the effects of abandonment are retained in
the long-term.
Acknowledgements
This project was supported by the Italian Ministry of Agricultural, Food and Forestry Policies, State Forestry Corps, within the
framework of the research agreement No. 767/2008 with the University of Padova. The authors express their thanks to Giovanni
Barazzutti, Simone Qualizza, Agata Scudo, Cristiana Colpi, Serena
Marte, Andrea Sgarbossa and Thomas Zinato for their assistance
in data collection and to Antonio Andrighetti and Franco Viola for
their support coordinating the work.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.foreco.2012.01.032.
References
Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of
variance. Aust. Ecol 26, 32–46.
Anderson, M.J., Ellingsen, K.E., McArdle, B.H., 2006. Multivariate dispersion as a
measure of beta diversity. Ecol. Lett. 9, 683–693.
Andrich, O., 2005. Progetto Speciale Selvicoltura e Piano di Riordino Forestale. Parco
Nazionale delle Dolomiti Bellunesi, Feltre.
Becker, M., 1989. The role of climate on present and past vitality of silver fir forests
in the Vosges-mountains of northeastern France. Can. J. For. Res. 19, 1110–1117.
Bianchi, L., Paci, M., 2008. Dinamica evolutiva e gestione delle abetine toscane:
sintesi di quarant’anni di ricerche. Forest@ 5, 122–130.
Binkley, D., 1995. The influence of tree species on forest soils: processes and
patterns. In: Mead, D.J., Cornforth, I.S. (Eds.), Proceedings of the Trees and Soil
Workshop. Lincoln University Press, Agronomy Society of New Zealand,
Canterbury, pp. 1–33.
Boncina, A., 2000. Comparison of structure and biodiversity in the Rajhenav virgin
forest remnant and managed forest in the Dinaric region of Slovenia. Global
Ecol. Biogeogr. 9, 201–211.
Bottacci, A., 2009. La Riserva Naturale Integrale di Sasso Fratino: 1959–2009. 50
anni di conservazione della biodiversità. CFS/UTB Pratovecchio, Pratovecchio,
Arezzo.
Braun-Blanquet, J., 1932. Plant sociology. Mc-Graw Hill, New York.
Burrascano, S., Lombardi, F., Marchetti, M., 2008. Old-growth forest structure and
deadwood: are they indicators of plant species composition? A case study from
central Italy. Plant Biosyst. 142, 313–323.
Burrascano, S., Rosati, L., Blasi, C., 2009. Plant species diversity in Mediterranean
old-growth forests: a case study from central Italy. Plant Biosyst. 143, 190–200.
Calamini, G., Maltoni, A., Travaglini, D., Iovino, F., Nicolaci, A., Menguzzato, G.,
Corona, P., Ferrari, B., Di Santo, D., Chirici, G., Lombardi, F., 2011. Stand structure
attributes in potential Old-Growth Forests in the Apennines, Italy. Ital. For.
Mont. 66, 365–381.
Carey, A.B., Johnson, M.L., 1995. Small mammals in managed, naturally young and
old-growth forests. Ecol. Appl. 5, 336–352.
Castagneri, D., Garbarino, M., Berretti, R., Motta, R., 2010. Site and stand effects on
coarse woody debris in montane mixed forests of Eastern Italian Alps. For. Ecol.
Manage. 260, 1592–1598.
Christensen, M., Hahn, K., Ountford, E.P., Ódor, P., Standovár, T., Rozenbergar, D.,
Diaci, J., Wijdeven, S., Meyer, P., Winter, S., Vrska, T., 2005. Dead wood in
European beech (Fagus sylvatica) forest reserves. For. Ecol. Manage. 210, 267–
282.
De Caceres, M., Legendre, P., 2009. Associations between species and groups of sites:
indices and statistical inference. Ecology, 3566–3574.
Debeljak, M., 2006. Coarse woody debris in virgin and managed forest. Ecol. Indic. 6,
733–742.
Del Favero, R., Lasen, C., 1993. La vegetazione forestale del Veneto. Libreria Progetto,
Padova.
Dufrêne, M., Legendre, P., 1997. Species assemblages an indicator species: the need
for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366.
237
Ellenberg, H., Weber, H.E., Düll, R., Wirth, W., Werner, W., Paulissen, D., 1991.
Zeigerwerte von Pflanzen in Mitteleuropa. Scr Geobot 18, 1–248.
Fabbio, G., Merlo, M., Tosi, V., 2003. Silvicultural management in maintaining
biodiversity and resistance of forests in Europe – the Mediterranean region. J.
Environ. Manage. 67, 67–76.
Ferrai, S., Mazzucchi, M., 1981. La selvicoltura trentina dal dopoguerra: indirizzi e
risultati. Economia. Montana. 13 (7), 10–15.
Fridman, J., Walheim, M., 2000. Amount, structure, and dynamics of dead wood on
managed forestland in Sweden. For. Ecol. Manage. 131, 23–36.
Fujimori, T., 2001. Ecological and silvicultural strategies for sustainable forest
management. Elsevier, Amsterdam.
Gabrielli, A., 2003. Viaggio in Italia sulle tracce dell’abete bianco. Ann. Accad. Ital.
Sci. For. 52, 125–207.
Gärtner, S., Reif, A., 2004. The impact of forest transformation on stand structure
and ground vegetation in the southern Black Forest, Germany. Plant Soil 264,
35–51.
Gibb, H., Pettersson, R.B., Hiältén, J., Hilszczański, J., Ball, J.P., Johansson, T., Atlegrim,
O., Danell, K., 2006. Conservation-oriented forestry and early successional
saproxylic beetles: responses of functional groups to manipulated dead wood
substrates. Biol. Conserv. 129, 437–450.
Gilg, O., 2004. Forêts à caractére naturel: caractéristiques, conservation et suivi.
Cahiers Techniques de l’ATEN: 74. Montpellier.
Goodale, C.L., Aber, J.D., 2001. The long-term effects of land-use history on nitrogen
cycling in northern hardwood forests. Ecol. Appl. 11, 253–267.
Graae, B.J., Heskjaer, V.S., 1997. A comparison of understorey vegetation between
untouched and managed deciduous forest in Denmark. For. Ecol. Manage. 96,
111–123.
Green, P., Peterken, G.F., 1997. Variation in the amount of dead wood in the
woodlands of the Lower Wye Valley, UK in relation to the intensity of
management. For. Ecol. Manage. 98, 229–238.
Gunn, J.S., Hagan, J.M., 2000. Woodpecker abundance and tree use in uneven-aged
managed, and unmanaged, forest in northern Maine. For. Ecol. Manage. 126, 1–
12.
Hansen, A.J., Spies, T.A., Swanson, F.J., Ohmann, J.L., 1991. Conserving biodiversity in
managed forests. Lessons from natural forests. Bioscience 41, 382–392.
Harmon, M.E., Franklin, J.F., Swanson, F.J., Sollins, P., Gregory, S.V., Lattin, J.D.,
Anderson, N.H., Cline, S.P., Aumen, N.G., Sedell, J.R., Lienkaemper, G.W.,
Cromack, K., Cummins, K.W., 1986. Ecology of coarse woody debris in
temperate ecosystems. Adv. Ecol. Res. 15, 133–302.
Hellrigl, B., 1986. La composizione dendrologica. In: Hellrigl, B. (Ed.), Nuove
metodologie nella elaborazione dei piani di assestamento dei boschi. Istituto
per lo Sviluppo Economico dell’Appennino Centro-Settentrionale, Bologna, pp.
444–445.
Heuze, P., Schnitzler, A., Klein, F., 2005. Consequences of increased deer browsing
winter on silver fir and spruce regeneration in the Southern Vosges mountains:
implications for forest management. Ann. For. Sci. 62, 175–181.
Heywood, V.H., Watson, R.T., 1995. Global biodiversity assessment. Cambridge
University Press, Cambridge, United Kingdom.
Hurlbert, S.H., 1984. Pseudoreplication and the design of ecological field
experiments. Ecol. Monogr. 54, 187–211.
Johann, E., 2007. Traditional forest management under the influence of science and
industry: the story of the alpine cultural landscapes. For. Ecol. Manage. 249, 54–
62.
Kirby, K.J., Webster, S.D., Antczak, A., 1991. Effects of forest management on stand
structure and the quantity of fallen dead wood: some British and Polish
examples. For. Ecol. Manage. 43, 167–174.
Kuuluvainen, T., Penttinen, A., Leinonen, K., Nygren, M., 1996. Statistical
opportunities for comparing stand structural heterogeneity in managed and
primeval forests: an example from boreal spruce forest in southern Finland.
Silva Fenn. 30, 315–328.
Lasen, C., Scariot, A., Sitzia, T., 2008. Natura 2000 Habitats map, forest types and
vegetation outline of Val Tovanella Nature Reserve. In: Hardersen, S., Mason, F.,
Viola, F., Campedel, D., Lasen, C., Cassol, M. (Eds.), Research on the natural
heritage of the reserves Vincheto di Celarda and Val Tovanella (Belluno
province, Italy). Conservation of two protected areas in the context of a LIFE
Project, Arti Grafiche Fiorini, Verona, pp. 325–334.
Lavorel, S., Grigulis, K., McIntyre, S., Williams, N.S.G., Garden, D., Dorrough, J.,
Berman, S., Quétier, F., Thébault, A., Bonis, A., 2008. Assessing functional
diversity in the field - methodology matters. Funct Ecol 134–147.
Lavorel, S., Grigulis, K., McIntyre, S., Williams, N.S.G., Garden, D., Dorrough, J.,
Berman, S., Quétier, F., Thébault, A., Bonis, A., 2006. Assessing functional
diversity in the field – methodology matters. Funct. Ecol., 134–147.
Liu, T. (Ed.), 1971. A monograph of the genus Abies. Department of Forestry, College
of Agriculture, National Taiwan University, Taipei, Taiwan.
Lombardi, F., Lasserre, B., Tognetti, R., Marchetti, M., 2008. Deadwood in relation to
stand management and forest type in Central Apennines (Molise, Italy).
Ecosystems 11, 882–894.
Maesano, M., Giongo Alves, M., Ottaviano, M., Marchetti, M., 2010. Prima analisi a
livello nazionale per l’identificazione delle High Conservation Value Forests
(HCVFs). Forest@ 8, 22–34.
Málek, J., 1981. Problematik der Okologie der Tanne (Abies alba Mill.) and ihres
Sterbens in der ČSSR. Forstwiss. Cent. bl. 100, 170–174.
Marage, D., Lemperiere, G., 2005. The management of snags: a comparison in
managed and unmanaged ancient forests of the Southern French Alps. Ann. For.
Sci. 62, 135–142.
238
T. Sitzia et al. / Forest Ecology and Management 270 (2012) 232–238
Marchetti, M., Tognetti, R., Lombardi, F., Chiavetta, U., Palumbo, G., Sellitto, M.,
Colombo, C., Iovieno, P., Alfani, A., Baldantoni, D., Barbati, A., Ferrari, B.,
Bonacquisti, S., Capotorti, G., Copiz, R., Blasi, C., 2010. Ecological portrayal of
old-growth forests and persistent woodlands in the Cilento and Vallo di Diano
National Park (southern Italy). Plant Biosyst. 144, 1–18.
Marshall, P.L., Davis, G., LeMay, W.M., 2000. Using line intersect sampling for coarse
woody debris. Research Section, Vancouver Forest Region, Vancouver (Canada).
Maser, C., Anderson, R., Cromack, J.K., Williams, J.T., Martin, R.E., 1979. Dead and
down woody material. In: Thomas, J.W. (Ed.), Wildlife habitats in managed
forests: the Blue Mountains of Oregon and Washington. Wildlife Management
Institute, Washington DC, pp. 78–95.
Mayer, H., 1979. Il ruolo selvicolturale dell’abete nelle Alpi e Prealpi centroorientali. Annali Ann. Accad. Ital. Sci. For. 28, 245–265.
McAlister, S., 1995. Species interactions and substrate-specificity among loginhabiting bryophyte species. Ecology 76, 2184–2195.
MCPFE, 1998. Follow-up reports on the ministerial conferences on the protection of
forests in Europe, 2. Third Ministerial Conference on the Protection of Forests in
Europe, Liaison Unit, Lisbon.
Millar, R.B., Anderson, M.J., 2004. Remedies for pseudoreplication. Fish. Res. 70,
397–407.
Motta, R., Garbarino, F., 2003. Stand history and its consequences for the present
and future dynamic in two silver fir (Abies alba Mill.) stands in the high Pesio
Valley (Piedmont, Italy). Ann. For. Sci. 60, 361–370.
Motta, R., Berretti, R., Lingua, E., Piussi, P., 2006. Coarse woody debris, forest
structure and regeneration in the Valbona Forest Reserve, Paneveggio, Italian
Alps. For. Ecol. Manage. 235, 155–163.
Motta, R., Maunaga, Z., Berretti, R., Castagneri, D., Lingua, E., Meloni, F., 2008. La
Riserva forestale di Lom (Repubblica di Bosnia Erzegovina): descrizione,
caratteristiche, struttura di un popolamento vetusto e confronto con
popolamenti stramaturi delle Alpi italiane. Forest@ 5, 100–111.
Motta, R., Berretti, R., Castagneri, D., Lingua, E., Nola, P., Vacchiano, G., 2010. Stand
and coarse woody debris dynamics in subalpine Norway spruce forests
withdrawn from regular management. Ann. For. Sci., 67.
Oksanen, J., Guillaume Blanchet, F., Kindt, R., Legendre, P., O’Hara, R.B., Simpson,
G.L., Solymos, P., Stevens, M.H.H., Wagner, H., 2011. vegan: Community Ecology
Package. R package version 1. 17–6.
Ozenda, P., 1985. La végétation de la chaîne alpine dans l’espace montagnard
européen. Masson, Paris.
Paillet, Y., Berges, L., Hjalten, J., Odor, P., Avon, C., Bernhardt-Romermann, M.,
Bijlsma, R.J., De Bruyn, L., Fuhr, M., Grandin, U., Kanka, R., Lundin, L., Luque, S.,
Magura, T., Matesanz, S., Meszaros, I., Sebastia, M.T., Schmidt, W., Standovar, T.,
Tothmeresz, B., Uotila, A., Valladares, F., Vellak, K., Virtanen, R., 2010.
Biodiversity differences between managed and unmanaged forests: metaanalysis of species richness in Europe. Conserv. Biol. 24, 101–112.
Parviainen, J., Bucking, W., Vandekerkhove, K., Schuck, A., Paivinen, R., 2000. Strict
forest reserves in Europe: efforts to enhance biodiversity and research on
forests left for free development in Europe (EU-COST-Action E4). Forestry 73,
107–118.
Paterson, S., Lello, J., 2003. Mixed models: getting the best use of parasitological
data. Trends in Parasitol. 19, 370–375.
Pettenella, D., Secco, L., 2006. Small-scale forestry in the Italian Alps: from mass
market to territorial marketing. In: Wall, S. (Ed.), Small-scale Forestry and Rural
Development: The intersection of ecosystems, economics and society. IUFRO,
Galway, Ireland, pp. 398–408.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., the R Development Core Team, 2010.
nlme: Linear and Nonlinear Mixed Effects Models. R package version 3. 1–97.
Piussi, P., 1991. Forestry in the Italian Alps: ecological, sociological and economic
problems. For. Chron. 67, 366–369.
R Development Core Team, 2009. R: a language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna, Austria.
Roberts, D.W., 2010. labdsv: ordination and multivariate analysis for ecology. R
package version 1. 4–1.
Ruffner, C.M., Abrams, M.D., 1998. Relating land-use history and climate to the
dendroecology of a 326-year-old Quercus prinus talus slope forest. Can. J. For.
Res. 28, 347–358.
Sagnard, F., Barberot, C., Fady, B., 2002. Structure of genetic diversity in Abies alba
Mill. from southwestern Alps: multivariate analysis of adaptive and nonadaptive traits for conservation in France. For. Ecol. Manage. 157, 175–189.
Schaffers, A.P., Sýkora, K.V., 2000. Reliability of Ellenberg indicator values for
moisture, nitrogen and soil reaction: a Comparison with field measurements. J.
Veg. Sci. 11, 225–244.
Schmidt, W., 2005. Herb layer species as indicators of biodiversity of managed and
unmanaged beech forests. For. Snow Landsc. Res. 79, 111–125.
Schnitzler, A., Borleab, F., 1998. Lessons from natural forests as keys for sustainable
management and improvement of naturalness in managed broadleaved forests.
For. Ecol. Manage. 109, 293–303.
Senn, J., Suter, W., 2003. Ungulate browsing on silver fir (Abies alba) in the Swiss
Alps: beliefs in search of supporting data. For. Ecol. Manage. 181, 151–164.
Sollins, P., 1982. Input and decay of coarse woody debris in coniferous stands in
western Oregon and Washington. Can. J. For. Res. 12, 18–28.
Stokland, J.N., 2001. The coarse woody debris profile: an archive of recent forest
history and an important biodiversity indicator. Ecol. Bull. 49, 71–83.
Susmel, L., 1958. Piano di riordinamento della proprietà silvo-pastorale Costantini
in Val Tovanella (1958–1967). Azienda di Stato per le Foreste Demaniali, Ufficio
di Belluno, Belluno.
Susmel, L., 1981. Normalizzazione delle foreste alpine. Liviana Editrice S.p.A,
Padova.
Tichý, L., 2005. New similarity indices for the assignment of relevés to the
vegetation units of an existing phytosociological classification. Plant Ecol. 179,
67–72.
Uotila, A., Maltamo, M., Uuttera, J., Isomäki, A., 2001. Stand structure in seminatural and managed forests in eastern Finland and Russian Karelia. Ecol. Bull.
49, 149–158.
Van Wagner, C.E., 1982. Practical aspects of the Line Intersect Method. Petawawa
National Forestry Institute, Canadian Forest Service, Chalk River (Canada).
Vanbergen, A.J., Woodcock, B.A., Watt, A.D., Niemela, J., 2005. Effect of land-use
heterogeneity on carabid communities at the landscape scale. Ecography 28, 3–16.
Viola, F., Campedel, D., Toffolet, L., 2008. Introduction, In: Hardersen, S., Mason, F.,
Viola, F., Campedel, D., Lasen, C., Cassol, M. (Eds.), Research on the natural
heritage of the reserves Vincheto di Celarda and Val Tovanella (Belluno
province, Italy). Conservation of two protected areas in the context of a Life
Project. Arti Grafiche Fiorini, Verona, pp. 17–24.
Vrska, T., Adam, D., Hort, L., Kolar, T., Janik, D., 2009. European beech (Fagus sylvatica
L.) and silver fir (Abies alba Mill.) rotation in the Carpathians – A developmental
cycle or a linear trend induced by man? For. Ecol. Manage. 258, 347–356.
White, M.A., Mladenoff, D.J., 1994. Old-growth forest landscape transitions from
pre-European settlement to present. Landscape Ecol. 9, 191–205.
Zar, J.H., 1999. Biostatistical Analysis, fourth ed. Prentice Hall, NJ, USA.