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Article
Influence of Forest Stand Structure and Competing Understory
Vegetation on Ash Regeneration—Potential Effects of
Ash Dieback
Susanne Jochner-Oette 1,*, Tanja Rohrer 1, Anna-Katharina Eisen 1, Selina Tönnes 1and Barbara Stammel 2
Citation: Jochner-Oette, S.; Rohrer,
T.; Eisen, A.-K.; Tönnes, S.; Stammel,
B. Influence of Forest Stand Structure
and Competing Understory
Vegetation on Ash Regeneration—
Potential Effects of Ash Dieback.
Forests 2021,12, 128.
https://doi.org/10.3390/f12020128
Received: 8 December 2020
Accepted: 21 January 2021
Published: 24 January 2021
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1Physical Geography/Landscape Ecology and Sustainable Ecosystem Development,
Catholic University of Eichstätt-Ingolstadt, 85072 Eichstätt, Germany; tanja_rohrer@web.de (T.R.);
anna-katharina.eisen@ku.de (A.-K.E.); selina.toennes@ku.de (S.T.)
2Floodplain Institute, Catholic University of Eichstätt-Ingolstadt, 85072 Eichstätt, Germany;
barbara.stammel@ku.de
*Correspondence: susanne.jochner@ku.de; Tel.: +49-8421-9321742
Abstract:
Background and Objectives: The existence of common ash (Fraxinus excelsior) in Europe is
severely endangered by ash dieback. To support its future sustainability, it is essential to improve
the natural ash regeneration. The main aim of this study was to investigate the influence of light
conditions, conceivably influenced by stand structure/ash dieback, on ash regeneration and the
competition between ash seedlings and species growing in the understory. Materials and Methods:
We selected 40 plots in a riparian forest located in Bavaria, Germany. Light-related variables (Leaf
Area Index, gap fraction) were gathered with fish-eye photography, whereas other environmental
factors were derived from vegetation surveys (Ellenberg indicator values). We assessed vegetation
parameters such as species’ richness and coverage of the herb layer to account for competition with
ash seedlings. Results: Our results indicate that ash regeneration is favoured under shady conditions.
The majority of other abiotic factors were not statistically associated with the analysed ash metrics. In
contrast, the coverage of grass was negatively related to LAI and positively to gap fraction. Higher
herb and grass coverages were linked to a suppression of ash regeneration. A higher litter coverage
was associated with a higher frequency of ash seedlings. Nonparametric partial correlation analyses
demonstrated the influence of light and stressed that litter coverage is of particular importance.
Conclusions: We conclude that gaps, inter alia induced by ash dieback, favour grass invasion. In turn,
this invasion might suppress regeneration of ash. In this regard, rapid silvicultural management
such as reforestation of gaps after dieback of mature trees is recommended. The influence of litter
on interspecific competition during growth should be also considered. The pace of dieback might
additionally influence the timing and quantity of litter accumulation; thus, further research should
also focus on these interrelations.
Keywords:
Fraxinus excelsior L.; grass; herb layer; light conditions; natural regeneration; riparian forest
1. Introduction
The broad-leaved common ash (Fraxinus excelsior L.) is a widespread tree species in
Europe. Due to its flood tolerance, it is one of the main tree species in floodplain forest
ecosystems [
1
,
2
]. Forestry faces major challenges in the management of riparian forests as
some species are economically unattractive (e.g., poplar, willows), while others are exposed
to major diseases (e.g., elm) [
3
]. For a long period, many ashes have been planted in order
to revalue mixed forest ecosystems economically and ecologically [
4
]. The importance
of ash—besides its ecological relevance—results from valuable wood characteristics such
as stability and elasticity, monopodial but also rapid vertical growth [
5
,
6
]. Their roots
dominate in the upper mineral soil horizon, forcing roots of other species such as beech
downwards and allowing ashes to be the first acquiring infiltrated water [
7
,
8
]. Thus, ash
Forests 2021,12, 128. https://doi.org/10.3390/f12020128 https://www.mdpi.com/journal/forests
Forests 2021,12, 128 2 of 12
is characterized by a high drought tolerance and is able to withstand high temperatures,
making it an optimal tree species under climate change conditions [9].
The abundance of ash is currently declining due to the fungus Hymenoscyphus fraxineus,
an invasive pathogen from East Asia [
10
,
11
]. First symptoms were already detected in
the 1990s in Poland, but the causal agent could not been identified [
12
]. Only in 2006,
the pathogen associated with ash dieback was identified as a new anamorphic form
(Chalara fraxinea) of the fungus [
13
]. Now the disease is spreading over almost all of
Europe [
14
,
15
]. The ascomycete infests the tree through its leaves or shoots [
16
], which
results in dieback of branches and twigs and dwarf growth, and it may even lead to a
gradual death of the tree within a few years [
14
]. Ash dieback mostly affects trees with an
average or below-average size, which suggests that individual tree resistance is related to
growth potential or tree vigour [
17
]. It is also known that a strong genetic variation in the
susceptibility to ash dieback exists [18].
In the past, the high regeneration rate of ashes was discussed as a problem for mixed
stands [
19
]. The well-appointed root system of ashes in combination with the high germina-
tion potential even under dense canopies are an obvious advantage over other tree species
such as beech (not in riparian forests), oaks or poplars. In consideration of the current
threat of ash dieback and in order to support the future viability and sustainability of ash,
it is essential to improve its natural regeneration. It is the product of natural selection,
which could offer opportunities to fight the disease [
4
,
20
]. Those seedlings from the natural
regeneration, which are able to withstand interspecific or intraspecific competition, might
present resistant phenotypes, which are also able to cope with the disease. Considering a
high mortality of ash trees in affected areas along with a genetic variation in susceptibility
may eventually result in more resistant juvenile ash trees [
21
]. A lower mortality and
damage of seedlings of populations in Lithuania was already attributed to such a selection
process [
22
]. Thus, breeding of resistant trees in future might be a powerful opportunity
for the endangered ash [9,21].
Ash is usually characterized by a high seed production and regeneration rate. In
Belgium, this rate was quantified with ca. 150,000 individuals per hectare under particularly
good site conditions [
23
,
24
]. Ash juveniles have a high shade tolerance, whereas older trees
are characterized by a higher light demand [
6
,
8
,
25
]. Therefore, ash is associated with a
high juvenile survival rate in case of low incidence of light and a pronounced increase in
height under amplified light availability.
Grass species in forests compete with tree seedlings or herbaceous plants for light,
water and nutrients, which may result in allelopathy, mechanical obstruction of the roots
or aboveground overgrowing [
26
,
27
]. Disturbances such as the dieback or the death of
a large canopy tree can result in suddenly changed light conditions and subsequently in
intense competition for above- and below-ground resources [
28
]. In the light of ash dieback,
the crown transparency of old ash stocks represents a challenge for forest management,
because grass invasion may additionally suppress ash regeneration [
29
,
30
]. Ash dieback
might not only lead to an abundant growth of grass but also to an increasing growth of
other light-demanding tree seedlings. In Lithuania’s forests, the disease already induced
comprehensive changes in forest structure and species composition. Secondary succession
in former ash-dominated locations resulted in a different tree composition consisting of
birch and grey alder [
31
]. However, the effects on the composition of the herb layer due to
changes in abiotic factors (e.g., light conditions) and biotic factors (e.g., competition) are
largely unexplored.
In this study, we examine the influence of light-related variables, conceivably also
modified by ash dieback, on the abundance of ash seedlings in a riparian forest in Southern
Germany. In addition, we consider statistical relationships with other environmental
factors, i.e., soil moisture, nutrient availability and soil reaction.
We compared the density and proportion of ash seedling to other seedlings growing
in the herb layer to account for competition. Thus, the main aim was to test whether
light availability is a key parameter for the development of natural ash regeneration and
Forests 2021,12, 128 3 of 12
to identify especially the influence of structural pattern of understorey vegetation on
their occurrence.
2. Study Area
Data were collected in a floodplain forest along the Danube between Neuburg and
Ingolstadt (Bavaria, Germany; Figure 1). The study area is rather flat and situated at about
375 m a.s.l. According to Köppen-Geiger’s climate classification, the climate is oceanic
(Cfb) [
32
]. The average annual precipitation is 715 mm and mean annual temperature is
7.8 ◦C (1961–1990) [33,34].
Forests 2021, 12, x FOR PEER REVIEW 3 of 12
We compared the density and proportion of ash seedling to other seedlings growing
in the herb layer to account for competition. Thus, the main aim was to test whether light
availability is a key parameter for the development of natural ash regeneration and to
identify especially the influence of structural pattern of understorey vegetation on their
occurrence.
2. Study Area
Data were collected in a floodplain forest along the Danube between Neuburg and
Ingolstadt (Bavaria, Germany; Figure 1). The study area is rather flat and situated at about
375 m a.s.l. According to Köppen-Geiger’s climate classification, the climate is oceanic
(Cfb) [32]. The average annual precipitation is 715 mm and mean annual temperature is
7.8 °C (1961–1990) [33,34].
Due to the proximity to the Danube, young riparian sediments of the last Danube ter-
race predominate [35]. Soils are influenced by former flooding and consist of overlaying
calcareous, nutrient-rich substrate of mainly fine-grained alluvial loam [36]. The location
allows for favourable growth conditions related to all types of floodplain forest trees [37].
Ca. 25% of the prevailing canopy trees belong to the species Acer pseudoplatanus.
Other tree species with high abundances (ca. 15%) are Fraxinus excelsior and Carpinus bet-
ulus, and with lower abundances (<15%) Quercus robur, Tilia cordata, Ulmus minor and Acer
campestre. Symptoms of ash dieback were frequently observed: 48.5% of the adult ash trees
near the plots were characterized as (severely) damaged with a leaf loss greater than 30%,
according to the scoring system of Lenz et al. (2012) [38]. In contrast, 33.3% of the adult
ash trees were only slightly affected and 18.2% did not show any symptoms of ash die-
back. In contrast, less than 10% of the ash seedlings growing within the selected plots were
associated with symptoms related to ash dieback.
Figure 1. Localization of the study site (black rectangle) in Bavaria, Germany. (Basis data: Bundesamt für Kartographie
und Geodäsie, Germany—DEM: 200m, GK3; DLM: 250m, GK3, 2019).
3. Materials and Methods
Data were collected within an area known for the occurrence of ash regeneration in
40 round plots, which were sized with a diameter of three meters (7.1 m
2
) in order to cover
and characterize a large area of the forest floor. To obtain results for the whole range of
the floodplain, forest areas on both sides of the river were investigated. The 20 plots in the
Figure 1.
Localization of the study site (black rectangle) in Bavaria, Germany. (Basis data: Bundesamt für Kartographie und
Geodäsie, Germany—DEM: 200 m, GK3; DLM: 250 m, GK3, 2019).
Due to the proximity to the Danube, young riparian sediments of the last Danube
terrace predominate [
35
]. Soils are influenced by former flooding and consist of overlaying
calcareous, nutrient-rich substrate of mainly fine-grained alluvial loam [
36
]. The location
allows for favourable growth conditions related to all types of floodplain forest trees [37].
Ca. 25% of the prevailing canopy trees belong to the species Acer pseudoplatanus. Other
tree species with high abundances (ca. 15%) are Fraxinus excelsior and Carpinus betulus, and
with lower abundances (<15%) Quercus robur,Tilia cordata,Ulmus minor and Acer campestre.
Symptoms of ash dieback were frequently observed: 48.5% of the adult ash trees near the
plots were characterized as (severely) damaged with a leaf loss greater than 30%, according
to the scoring system of Lenz et al. (2012) [
38
]. In contrast, 33.3% of the adult ash trees were
only slightly affected and 18.2% did not show any symptoms of ash dieback. In contrast,
less than 10% of the ash seedlings growing within the selected plots were associated with
symptoms related to ash dieback.
3. Materials and Methods
Data were collected within an area known for the occurrence of ash regeneration in
40 round plots, which were sized with a diameter of three meters (7.1 m
2
) in order to cover
and characterize a large area of the forest floor. To obtain results for the whole range of
the floodplain, forest areas on both sides of the river were investigated. The 20 plots in
the southern part were located in the actual floodplain but were rarely flooded due to its
elevation, whereas the 20 plots in the northern part were located in the former floodplain
where possible flooding of the Danube is retained by a dam. Plots at these two sites were
Forests 2021,12, 128 4 of 12
selected randomly, each in a forest sector of 9 ha (southern part) and of 4 ha (northern part)
where ash frequently occurs (abundance of 15%). The health status of adult ash trees next
to these plots was not used as criterion for plot selection. Adult tree density and structure
of the forest differ within the area, among others due to ash dieback of individual trees.
Thus, the canopy openness of our plots varies greatly.
We performed vegetation surveys in June and July 2019 determining the abundance
of each species in the herb layer according to the scale of Londo (1975) [
39
]. In addition, we
counted the number of individuals of the herb layer and we estimated the coverage of soil
and litter as well as the grass coverage of the vegetation cover (plot area minus soil and
litter coverage) in %. The distance between the plot centre and the nearest adult ash tree
was recorded.
Data on ash regeneration were of particular interest: We counted the number of ash
seedlings within each plot to calculate the density of ash regeneration (abbreviated “ash
seedling density”, (m
−2
)), assessed the proportion of ash individuals among all prevailing
individuals in the herb layer (abbreviated “proportion of ash”, (%)) and the percentage of
ash seedlings among all tree seedlings (abbreviated “ash % among seedlings”, (%)). These
variables were used as dependent variables in statistical analyses.
The natural abiotic conditions of a site determine species occurrence, especially of
the herb layer. Therefore, species composition was analysed using Ellenberg indicator
values [
40
]. In our study, we used the indicators for soil reaction (R) and nutrients (N)
on a scale from 1 (low) to 9 (high), and for the moisture indicator (M) from 1 to 12. For
each plot, the cover-weighted average of these indicator values of herb-layer species was
calculated. Other indicators were ignored, since they are more suitable for larger scales
(temperature and continentality) or were measured directly (light). The Leaf Area Index
(LAI) of each plot was evaluated by digital hemispherical photography (Canon EOS 60
D (18 MP), 4.5 mm lens (Sigma model EX CD)). This dimensionless index describes the
one-sided area of photosynthetically active material per ground surface area [
41
]. The
photographs were taken during overcast sky conditions between 25 June and 12 July 2019
and were analysed using the software HemiView 2.1 [
42
]. In addition to LAI, we included
gap fraction (G), which is defined as the fraction of visible sky [
43
] and can vary between
0% (completely obscured sky) and 100% (completely visible sky).
Statistical analyses were performed using IBM SPSS Statistics 25. If data did not
meet the statistical requirements, i.e., normal distribution assessed using the Kolmogorow
Smirnow test, nonparametric tests were applied, which included Spearman’s rank order
correlation. In a second step, we investigated the effect of LAI when controlling for the
most important biotic variable (i.e., coverage of litter) by nonparametric partial correlation
analysis. We applied the Mann–Whitney U test to compare mean values for plots, which
were categorized in classes according to the proportion of ash in the herb layer.
4. Results
4.1. Ash Metrics and Abiotic and Biotic Variables
We observed a mean density of 2.2 ash seedlings m
−2
(range 0.1–8.5) at the selected
plots (Table 1). On average, 13.2% (range 0.5%–41.6%) of the recorded individuals in
the herb layer were ash seedlings and 38.3% (range 0%–100%) of all occurring seedlings
belonged to ash. The mean distance to the nearest adult ash tree was 13.5 m (range
0.8–50 m).
Forests 2021,12, 128 5 of 12
Table 1.
Collected variables and their mean, minimum, maximum values including standard deviation. LAI: Leaf Area
Index, G: gap fraction (%), M, R, N: Ellenberg indicator values for soil moisture, reaction, and nutrients, N: number, dist.
ash (m): distance to the nearest adult ash tree.
Variable Category Statisitics Ash Seedling
Density [m−2]
Proportion
of Ash
Ash % among
Seedlings
Ash regeneration
metrics
Mean 2.2 13.2 38.3
Standard
deviation 2.0 11.3 23.4
Minimum 0.1 0.5 0
Maximum 8.5 41.6 100
LAI G M R N
Variables related to
light conditions and
abiotic factors
Mean 2.1 15.2 5.4 7.1 6.7
Standard
deviation 0.5 6.4 0.6 0.2 0.8
Minimum 1.0 5.5 3.7 6.5 4.4
Maximum 3.4 34.8 6.0 7.7 8.0
Dist. Ash NSpecies Herb Layer % Litter % Soil % Grass %
Variables related to
vegetation and biotic
factors
Mean 13.5 10.3 73.1 16.7 3.4 36.2
Standard
deviation 17.6 2.5 20.8 19.8 6.5 26.0
Minimum 0.8 4.0 18.0 0.0 0.0 0.0
Maximum 50.0 17.0 98.0 75.0 40.0 88.4
The descriptive statistics related to LAI and gap fraction confirmed a wide range of
different light conditions: LAI varied between 1.0 and 3.4 (mean 2.1) and gap fraction
between 6.4% and 34.8% (mean 15.2%).
The Ellenberg indicator for soil moisture (M) varied between 3.7 and 6.0 (mean 5.4).
The means of the other indicator values of the herbal layer were 7.1 (range 6.5–7.7) for soil
reaction (R) and 6.7 (range 4.4–7.9) for nutrients (N) (Table 1).
An average of 10 different herb species (range 4–17) was found in the herb layer, which
covers a mean surface of 73.1% (range 18%–98%) of the plot area (mean litter coverage
16.7%, range 0%–75% and mean soil coverage 3.4%, range 0%–40%). The coverage of grass
species varied greatly among plots with values between 0% and 88.4% (mean 36.2%).
Table 2lists all species observed in the understory and their respective coverage at
the 40 plots. In total, 57 species were recorded but only three of them were associated
with a coverage greater than 6%: Aegopodium podagraria (11.9%), and the two tree seedlings
Acer pseudoplatanus (6.5%, N= 655) and Fraxinus excelsior (6.4%, N= 634).
4.2. Relationship between Ash Regeneration, Grass Cover and Abiotic and Biotic Variables
Ash regeneration is favoured under lower light incidence. This was documented by a
positive correlation between LAI and the ash seedling density or the proportion of ashes
(r
s
= 0.400, p= 0.011 and r
s
= 0.300, p= 0.037), and the negative correlation between ash
seedling density and gap fraction (rs=−0.385, p= 0.014).
Soil reaction showed a statistically significant correlation with ash density (r
s
=
−
0.330,
p= 0.038) and proportion of ash (rs=−0.355, p= 0.025). All other abiotic factors were not
statistically associated with the analysed ash metrics.
The coverage of grass was negatively related to LAI (r
s
=
−
0.346, p= 0.029) and
positively to gap fraction (r
s
= 0.319, p= 0.045) and thus showed the opposite pattern of
ash regeneration. Figure 2a,b visualizes the relationships between gap fraction and the
proportion of ash and coverage of grass. Steep regression slopes point to great changes in
Forests 2021,12, 128 6 of 12
the proportion of ash and grass coverage under small variations of gap fraction. However,
r
2
remains quite low (<0.2) and statistical significance is only given for the relationship
between gap fraction and grass coverage.
Table 2.
Observed species and their coverage in the understorey at the 40 studied plots, t = tree,
s = shrub, h = herb, l = liana.
Species Coverage % Species Coverage %
Aegopodium podagraria (h) 11.9 Juniperus communis (s) 0.2
Acer pseudoplatanus (t) 6.5 Vincetoxicum hirundinaria (h) 0.1
Fraxinus excelsior (t) 6.4 Aconitum napellus (h) 0.1
Acer campestre (t) 2.1 Anthriscus sylvestris (h) 0.1
Rubus silvaticus (s) 1.3 Corylus avellana (s) 0.1
Carpinus betulus (t) 1.1 Galeopsis tetrahit (h) 0.1
Viola odorata (h) 1.1 Galium mollugo (h) 0.1
Cornus mas (s) 1.0 Glechoma hederacea (h) 0.1
Geum urbanum (h) 0.9 Hypericum perforatum (h) 0.1
Asarum europaeum (h) 0.8 Viburnum lantana (s) 0.1
Viola reichenbachiana (h) 0.7 Centaurea jacea (h) 0.1
Lonicera xylosteum (s) 0.6 Hieracium murorum (h) 0.1
Crataegus monogyna (s) 0.6 Hypericum hirsutum (h) 0.1
Galium aparine (h) 0.5 Lotus corniculatus (h) 0.1
Clematis vitalba (l) 0.4 Pimpinella saxifrage (h) 0.1
Cornus sanguinea (s) 0.4 Prunus padus (t) 0.1
Euphorbia cyparissias (h) 0.4 Rosa canina (s) 0.1
Quercus robur (t) 0.4 Veronica arvensis (h) <0.1
Ligustrum vulgare (s) 0.4 Clinopodium vulgare (h) <0.1
Paris quadrifolia (h) 0.4 Euphorbia amygdaloides (h) <0.1
Ranunculus nemorosus (h) 0.3 Lamium album (h) <0.1
Lamium maculatum (h) 0.3 Plantago lanceolata(h) <0.1
Mercurialis perennis (h) 0.3 Primula elatior (h) <0.1
Tilia cordata (t) 0.3 Prunella vulgaris (h) <0.1
Ulmus minor (t) 0.2 Salvia pratensis (h) <0.1
Circaea lutetiana (h) 0.2 Tilia platyphyllos (t) <0.1
Daphne mezereum (s) 0.2 Viburnum lantana (h) <0.1
Origanum vulgare (h) 0.2 Viola melissifolia (h) <0.1
Viola riviniana (h) <0.1
Forests 2021, 12, x FOR PEER REVIEW 7 of 12
Figure 2. Scatterplot visualisation of the relationships between gap fraction and proportion of ash (a) and coverage of grass (b).
The Mann–Whitney U test revealed that the mean grass coverage of selected classes
categorised by the proportion of ash seedlings among all prevailing individuals in the
herb layer (class 1: >15%, class 2: 7.5%–15%, class 3: <7.5%) was significantly different for
class 1 and 2 (p = 0.032), marginally significantly different for class 1 and 3 (p = 0.051), but
not significantly different for class 2 and 3 (p = 0.621). The mean grass coverage was 20.9%
for class 1, 40.0% for class 2 and 43.9% for class 3.
5. Discussion
In our 40 studied plots located in the floodplain forest and with a total size of 284 m2,
we registered 634 ash seedlings which is equivalent to 22,324 individuals per ha. Existing
literature documents an almost seven times higher regeneration rate of ash (150,000 indi-
viduals/ha) under favourable site conditions in a dense seminatural mixed hardwood for-
est in Belgium [23,24]. In our study, only seedlings of Acer pseudoplatanus (N = 655) were
found more frequently than ash seedlings. More than 80% of the adult ash trees growing
at our study site showed symptoms of ash dieback. Although we did not sample airborne
Hymenoscyphus fraxineus spores, we suppose that their concentration is high enough to
affect ashes from all age classes. However, only 10% of the ash regeneration showed
symptoms of ash dieback.
5.1. Relationships between Variables Related to Light Conditions and Ash Regeneration
In the literature, it is well known that ash regeneration exhibits a remarkable shade
tolerance [25,44], which is lower for oak or maple [5]. However, ash transforms into a
light-demanding tree at an age of seven or eight [8]. A wide range of gap fraction (5.5% to
34.8%, see Table 1) characterized the studied plots. Plots associated with lower values of
gap fraction and therefore lower light levels on the ground had higher ash seedling den-
sities and a higher proportion of ash seedlings (Table 3). A coherent relationship was doc-
umented for LAI (c.f. N ash seedling).
Related to the magnitude of the correlation coefficients, we conclude that especially
LAI is the most appropriate measure for assessing the relation to ash regeneration. LAI
accounts for photosynthetic and transpirational surface of plant canopies [45] and might
therefore be suitable to account for the competition for light.
Figure 2.
Scatterplot visualisation of the relationships between gap fraction and proportion of ash (
a
) and coverage of
grass (b).
Forests 2021,12, 128 7 of 12
Higher herb and grass coverages were related to a suppression of ash regeneration,
regardless of the ash metric used but with highest correlation coefficients for ash seedling
density (cf. coverage of the herb layer: r
s
=
−
0.523, p= 0.001; cf. coverage of grass:
rs=−0.546
,p< 0.001). The coverage of soil was not significantly related to the ash re-
generation metrics. A higher litter coverage, however, was linked to increases in ash
regeneration with the highest correlation coefficient of r
s
= 0.674 (p< 0.001, proportion
of ash). Nonparametric partial correlation analyses that controlled for the effect of litter
coverage revealed that LAI is still significantly related to ash density (r
s
= 0.396, p= 0.014),
marginally significantly related to the proportion of ash among all individuals in the herb
layer (r
s
= 0.314, p= 0.055), but not significantly related to the percentage of ash among
seedlings (rs= 0.202, p= 0.224).
The coverage of grass was higher at plots with a higher coverage of the herb layer
(
rs= 0.571
,p< 0.001) and litter (r
s
= 0.457, p= 0.003). In turn, the coverage of grass was
lower at plots with higher soil coverage (rs=−0.347, p= 0.030).
There were no correlations between the distance to the nearest adult ash tree and
ash-regeneration metrics or the number of species found in the herb layer.
The Mann–Whitney U test revealed that the mean grass coverage of selected classes
categorised by the proportion of ash seedlings among all prevailing individuals in the herb
layer (class 1: >15%, class 2: 7.5–15%, class 3: <7.5%) was significantly different for class
1 and 2 (p= 0.032), marginally significantly different for class 1 and 3 (p= 0.051), but not
significantly different for class 2 and 3 (p= 0.621). The mean grass coverage was 20.9% for
class 1, 40.0% for class 2 and 43.9% for class 3.
5. Discussion
In our 40 studied plots located in the floodplain forest and with a total size of 284 m
2
,
we registered 634 ash seedlings which is equivalent to 22,324 individuals per ha. Existing
literature documents an almost seven times higher regeneration rate of ash (150,000 in-
dividuals/ha) under favourable site conditions in a dense seminatural mixed hardwood
forest in Belgium [
23
,
24
]. In our study, only seedlings of Acer pseudoplatanus (N= 655) were
found more frequently than ash seedlings. More than 80% of the adult ash trees growing at
our study site showed symptoms of ash dieback. Although we did not sample airborne
Hymenoscyphus fraxineus spores, we suppose that their concentration is high enough to
affect ashes from all age classes. However, only 10% of the ash regeneration showed
symptoms of ash dieback.
5.1. Relationships between Variables Related to Light Conditions and Ash Regeneration
In the literature, it is well known that ash regeneration exhibits a remarkable shade
tolerance [
25
,
44
], which is lower for oak or maple [
5
]. However, ash transforms into a
light-demanding tree at an age of seven or eight [
8
]. A wide range of gap fraction (5.5%
to 34.8%, see Table 1) characterized the studied plots. Plots associated with lower values
of gap fraction and therefore lower light levels on the ground had higher ash seedling
densities and a higher proportion of ash seedlings (Table 3). A coherent relationship was
documented for LAI (c.f. Nash seedling).
Related to the magnitude of the correlation coefficients, we conclude that especially
LAI is the most appropriate measure for assessing the relation to ash regeneration. LAI
accounts for photosynthetic and transpirational surface of plant canopies [
45
] and might
therefore be suitable to account for the competition for light.
Forests 2021,12, 128 8 of 12
Table 3.
Summary on Spearman’s rank correlation coefficients (r
s
) and p-values of all surveyed abiotic and biotic variables
related to ash-regeneration metrics and coverage of grass and herb layer. LAI: Leaf Area Index, G: gap fraction, M, R, N:
Ellenberg indicator values for soil moisture, reaction, and nutrients, dist. ash: distance to the next adult ash tree. Bold values
indicate significant correlations (p< 0.050).
Variables LAI G M R N
ash seedling density rs0.400 −0.385 0.036 −0.330 0.101
p0.011 0.014 0.842 0.038 0.533
proportion of ash rs0.330 −0.272 −0.190 −0.355 −0.197
p0.037 0.089 0.241 0.025 0.222
ash % among seedlings rs0.245 −0.172 −0.200 −0.204 0.014
p0.128 0.288 0.215 0.207 0.931
grass % rs−0.346 0.319 −0.354 0.157 −0.519
p0.029 0.045 0.025 0.333 0.001
herb % rs−0.164 0.203 −0.023 0.277 0.012
p0.311 0.210 0.887 0.084 0.939
dist. ash Nspecies herb % grass % litter % soil %
ash seedling density rs0.196 −0.042 −0.523 −0.546 0.619 0.112
p0.273 0.795 0.001 0.000 0.000 0.496
proportion of ash rs0.110 −0.088 −0.517 −0.323 0.674 0.159
p0.544 0.591 0.001 0.042 0.000 0.335
ash % among seedlings rs0.092 −0.005 −0.318 −0.360 0.444 −0.046
p0.609 0.977 0.046 0.023 0.005 0.782
grass % rs−0.228 0.059 0.571 10.457 −0.347
p0.202 0.719 0.000 0.003 0.030
herb % rs−0.134 0.214 1 0.571 0.809 −0.335
p0.457 0.186 0.000 0.000 0.037
5.2. Relationships between Other Abiotic Factors and Ash Regeneration
Besides the great importance of light, there might be other environmental factors
influencing regeneration such as soil nutrients [
28
]. Although soil characteristics are
assumed to vary only slightly between our investigated plots, the Ellenberg indicator
value for nutrients ranged between 4.4 and 7.9 (Table 1). However, this indicator was
not statistically significantly associated with any of the selected ash regeneration metrics.
The wide range of light availability seems to predominate the occurring variance in soil
conditions such as moisture or nutrient availability—factors that were reported to be of
importance in terms of the growth of seedlings [
46
]. In general, ash grows on a wide range
of soils but preferably on nutrient- and base-rich soils with pH values greater than 4.2 [
47
].
We found a significant and negative correlation between ash density or ash proportion
and soil reaction. However, the soil of our plots can be classified as base-rich (mean of the
reaction indicator: 7.1; range: 6.5–7.7, Table 1). Optimal conditions related to soil moisture
vary between very moist and fresh; however, slightly dry sites are also considered to be
suitable for the growth of ash [48].
5.3. Seed Availability Inferred by Distance Measures
The distance to the nearest adult tree ranged between 0.8 m and 50 m (mean 13.5 m,
Table 1), but was not significantly associated with ash-regeneration metrics. Thus, the
abundance of ash seedlings is not primarily linked to the occurrence of adult trees. Mean
distances for the dispersion of seeds from a 130-year-old mother tree (45 cm breast height
Forests 2021,12, 128 9 of 12
diameter) was estimated with 43.5 m [
49
]. An experimental study investigating seed
dispersal of a solitary ash tree documented that most of the seeds were found at 20 m
distance to the tree [
49
]. In our study, for only seven plots the distance to the next adult
tree was greater than the above-mentioned mean dispersion distance of 43.5 m. However,
mean values for ash-regeneration metrics did not differ significantly between sites with a
smaller (
≤
43.5 m) or greater distance (>43.5 m; data not shown). Thus, at our study site,
which is characterized by a high proportion of ash trees in the canopy layer (ca. 15%), seed
availability might not be a limiting factor.
5.4. Competition in the Herb Layer
Our results showed that high grass coverage is significantly accompanied by low ash
regeneration. In general, the coverage of grass was remarkably high (mean 36.2%,
Table 1
)
and exceeded up to 88.4%. Only four plots were associated with a complete absence of
grass; three of them were linked to a high proportion of ash seedlings (over 20% and up to
40%). Fast-growing grass species that compete for above- and below-ground resources have
a negative effect on the growth of young trees and therefore represent a major challenge for
forest management [
50
]. Plots with a high proportion of ash (>15%) had significantly lower
grass coverage than plots with a lower proportion (<7.5%). Grass coverage seems to be
favoured by a high translucency of light indicated by both correlations with LAI and gap
fraction (Table 3). Therefore, we assume that an ongoing damage of adult ash trees or other
factors that increase the light perception on the herb layer will favour grass and reduce the
amount of ash seedlings. Even if our results did not show clear correlations, herbaceous
species are also able to occupy the herb layer below canopy gaps quickly [
51
,
52
]. Due to
the generally higher species number of herb species compared to grasses and thus their
higher variance in light demand, herbaceous species might suppress ash regeneration at
sites with larger shaded areas as well.
In general, herbaceous species might have an advantage over tree seedlings in the
competition for soil nutrients [
53
]. In our study, we found that the coverage of the herb
layer was negatively correlated to the selected ash metrics (Table 3). Thus, an important
biotic factor exposes the competition among species growing on the ground layer of the
floodplain forest. The proportion of ash regeneration among other tree seedlings had a
negative relationship to the coverage of the herb layer. However, whether herbaceous
species suppress ash seedlings even more than other seedlings needs to be further studied.
5.5. Relationship between Litter and Ash Regeneration
The highest correlations were found between ash metrics and the coverage of litter
(e.g., c.f. proportion of ash seedlings r
s
= 0.674, Table 3). Being aware that statistical
correlations are not automatically causal relations, litter seems to suppress other species as
documented by the negative correlations with the coverage of grass and herb layer (
Table 3
)
and might favour the germination of ash seeds, also compared to other tree species (% of
ash among seedlings). Thus, the influence of litter on the interspecific competition during
growth is especially meaningful and associated with even higher correlation coefficients
compared to light-related variables (Table 3). Partial correlations revealed that controlling
for litter coverage reduces the effect of light (i.e., LAI) in magnitude. Light availability is
still of importance when ash density or the proportion ash seedlings among all individuals
in the herb layer are regarded. Considering the proportion of ash seedlings among all
prevailing seedlings, a high litter coverage seems to support ash seedlings in contrast
to others.
Strong and quickly intensifying symptoms of ash dieback might be rather associated
with a high quantity of leaf litter during the vegetation period, which could prevent from
grass invasion. A slower progress of the disease with a gradual leaf fall might not be linked
to higher quantities of litter within a short time span and thus does not favour the growth
of ash seedlings.
Forests 2021,12, 128 10 of 12
The tree species that dominate in our study area are characterized by a base- and
nutrient-rich litter (Fraxinus excelsior and Carpinus betulus) or an intermediate quality of
the litter (Acer pseudoplatanus) [
54
]. In general, base- and nutrient-rich litter increases
nutrient availability and diversity of soil habitats in mixed forest stands [
55
]. Hence, the
composition of canopy species influences the nutritional conditions of the soil (via leaf
litter) and in turn affects the composition of the understorey. In our study, the Ellenberg
indicator values for nutrients were not statistically significantly linked to ash regeneration.
Since ash seedlings are extremely tolerant to shade [
19
,
38
] large litter quantities might also
be beneficial for high survival rates compared to other tree seedlings.
6. Conclusions
The aim of this study was to investigate how light conditions and especially biotic
factors influence the occurrence of the natural regeneration of ash. We conclude that crown
gaps inter alia induced by mortality, leaf fall and damage of shoots caused by ash dieback
favour grass invasion. In turn, this implies a feedback loop since the invasion of grass
might suppress natural regeneration of ash, which might present resistant phenotypes
that are more successful in coping with the disease. In this regard, rapid silvicultural
management such as reforestation of gaps within the stand that occurred after dieback of
mature trees is recommended. Since we found that the coverage of litter on the ground
is an important factor influencing ash germination/growth, the speed of dieback might
also be a so-far overlooked component. However, investigations on that might not be
easy to trace in the natural environment and could be further addressed in controlled
experiments. Silvicultural management might increase litter cover to reduce grass cover
and to support ash regeneration. Further research on ash regeneration should especially
focus on neighbouring canopy trees and their characteristics related to the timing of leaf
fall, litter quantity/thickness and chemical composition of the leaf litter.
Author Contributions:
Conceptualization, S.J.-O.; methodology, S.J.-O. and B.S.; field work, T.R.;
data analyses, S.J.-O. and T.R.; writing—original draft preparation, T.R., S.J.-O. and B.S.; writing—
review and editing, S.J.-O.; B.S., A.-K.E. and T.R.; visualization, S.T. All authors have read and agreed
to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Data sharing not applicable.
Acknowledgments:
We gratefully acknowledge the Wittelsbacher Ausgleichsfonds for the permis-
sion to conduct scientific research in the riparian forest. We thank Rudolf Vierheilig and Christoph
Gabler for their support in the field and Johanna Jetschni for proofreading of the manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
References
1. Bayerische Landesanstalt für Wald und Forstwirtschaft. Die Regionale Natürliche Waldzusammensetzung Bayerns; LWF-Wissen 32;
Bayerische Landesanstalt für Wald und Forstwirtschaft: Freising, Germany, 2001.
2.
Mitchell, R.J.; Beaton, J.K.; Bellamy, P.E.; Broome, A.; Chetcuti, J.; Eaton, S.; Ellis, C.J.; Gimona, A.; Harmer, R.; Hester, A.J.; et al.
Ash dieback in the UK: A review of the ecological and conservation implications and potential management options. Biol. Conserv.
2014,175, 95–109. [CrossRef]
3. Dichtl, T.; Stöger, W. Auenwald im Klimawandel: Forstliche Forschung an Donau und Rhein. LWF Aktuell 2020,126, 28–29.
4. Enderle, R.; Fussi, B.; Lenz, H.D.; Langer, G.; Nagel, R.; Metzler, B. Ash dieback in Germany: Research on disease development,
resistance and management options. In Dieback of European Ash (Fraxinus spp.)—Consequences and Guidelines for Sustainable
Management; Vasaitis, R., Enderle, R., Eds.; European Cooperation in Science & Technology (COST): Uppsala, Sewden, 2017;
pp. 89–105, ISBN 978-91-576-8696-1.
5.
Tabari, K.M.; Lust, N.; Neirynk, J. Effect of light and humus on survival and height growth of ash (Fraxinus excelsior L.) seedlings.
Silva Gandav. 1998,63, 36–49. [CrossRef]
Forests 2021,12, 128 11 of 12
6.
Nüsslein, S. Waldbauliche Behandlung der Esche. In Beiträge zur Esche Fachtagung zum Baum des Jahres 2001; LWF-Wissen 34;
Bayerische Landesanstalt für Wald und Forstwirtschaft: Freising, Germany, 2002; pp. 41–43.
7.
Gulder, H.-J. Standortansprüche und Wurzelwerk der Esche. In Beiträge zur Esche Fachtagung zum Baum des Jahres 2001; LWF-
Wissen 34; Bayerische Landesanstalt für Wald und Forstwirtschaft: Freising, Germany, 2002; pp. 50–52.
8.
Schütz, J.P. Modellierung des Höhenwuchses der Esche in der Verjüngungsphase in Abhängigkeit von der Beschattung.
In Proceedings of the Jahrestagung 2004 des Deutschen Verbandes forstlicher Forschungsanstalten, Stift Schlägl, Austria,
24–26 May 2004; Deutscher Verband Forstlicher Forschungsanstalten: Göttingen, Germany, 2004; p. 109.
9.
Enderle, R.; Nakou, A.; Thomas, K.; Metzler, B. Susceptibility of autochthonous German Fraxinus excelsior clones to Hymenoscy-
phus pseudoalbidus is genetically determined. Ann. For. Sci. 2015,72, 183–193. [CrossRef]
10.
Zhao, Y.-J.; Hosoya, T.; Baral, H.-O.; Hosaka, K.; Kakishima, M. Hymenoscyphus pseudoalbidus, the correct name for Lambertella
albida reported from Japan. Mycotaxon 2013,122, 25–41. [CrossRef]
11.
Gross, A.; Holdenrieder, O.; Pautasso, M.; Queloz, V.; Sieber, T.N. Hymenoscyphus pseudoalbidus, the causal agent of European
ash dieback. Mol. Plant Pathol. 2014,15, 5–21. [CrossRef]
12. Przybyl, K. Fungi associated with necrotic apical parts of Fraxinus excelsior shoots. For. Pathol. 2002,32, 387–394. [CrossRef]
13.
Kowalski, T. Chalara fraxinea sp. nov. associated with dieback of ash (Fraxinus excelsior ) in Poland. For. Pathol.
2006
,36, 264–270.
[CrossRef]
14.
Pautasso, M.; Aas, G.; Queloz, V.; Holdenrieder, O. European ash (Fraxinus excelsior) dieback—A conservation biology challenge.
Biol. Conserv. 2013,158, 37–49. [CrossRef]
15.
Giongo, S.; Oliveira Longa, C.M.; Dal Maso, E.; Montecchio, L.; Maresi, G. Evaluating the impact of Hymenoscyphus fraxineus in
Trentino (Alps, Northern Italy): First investigations. iForest 2017,10, 871–878. [CrossRef]
16. Kowalski, T.; Holdenrieder, O. Pathogenicity of Chalara fraxinea. For. Pathol. 2009,39, 1–7. [CrossRef]
17.
Skovsgaard, J.P.; Thomsen, I.M.; Skovgaard, I.M.; Martinussen, T. Associations among symptoms of dieback in even-aged stands
of ash (Fraxinus excelsior L.). For. Pathol. 2010,40, 7–18. [CrossRef]
18.
McKinney, L.V.; Nielsen, L.R.; Hansen, J.K.; Kjær, E.D. Presence of natural genetic resistance in Fraxinus excelsior (Oleraceae) to
Chalara fraxinea (Ascomycota): An emerging infectious disease. Heredity 2011,106, 788–797. [CrossRef] [PubMed]
19.
Rysavy, T.; Roloff, A. Ursachen der Vereschung in Mischbeständen und Vorschläge zu ihrer Vermeidung. Forst Und Holz
1994
,49,
392–395.
20.
Metzler, B.; Enderle, R.; Karopka, M.; Toepfner, K.; Aldinger, E. Development of ash dieback in a provenance trial on different
sites in southern Germany. In Allgmeine Forst und Jagdzeitung; JD Sauerlaender ’s Verlag: Bad Orb, Germany, 2012; Volume 183,
pp. 168–180.
21.
McKinney, L.V.; Nielsen, L.R.; Collinge, D.B.; Thomsen, I.M.; Hansen, J.K.; Kjaer, E.D. The ash dieback crisis: Genetic variation in
resistance can prove a long-term solution. Plant Pathol. 2014,63, 485–499. [CrossRef]
22.
Pli
¯
ura, A.; Lygis, V.; Suchockas, V. Performance of twenty four European Fraxinus excelsior populations in three Lithuanian
progeny trials with a special emphasis on resistance to Chalara fraxinea. Balt. For. 2011,17, 17–34.
23. Tabari, K.M.; Lust, N. Monitoring of natural regeneration in a mixed deciduous forest. Silva Gandav. 1999,64. [CrossRef]
24.
Dobrowolska, D.; Hein, S.; Oosterbaan, A.; Wagner, S.; Clark, J.; Skovsgaard, J.P. A review of European ash (Fraxinus excelsior L.):
Implications for silviculture. Forestry 2011,84, 133–148. [CrossRef]
25.
Petritan, A.M.; von Lupke, B.; Petritan, I.C. Effects of shade on growth and mortality of maple (Acer pseudoplatanus), ash (Fraxinus
excelsior) and beech (Fagus sylvatica) saplings. Forestry 2007,80, 397–412. [CrossRef]
26.
Coomes, D.A.; Grubb, P.J. Impacts of root competition in forests and woodlands: A theoretical framework and review of
experiments. Ecol. Monogr. 2000,70, 171–207. [CrossRef]
27.
Flory, S.L.; Clay, K. Non-native grass invasion suppresses forest succession. Oecologia
2010
,164, 1029–1038. [CrossRef] [PubMed]
28.
Gilliam, F.S. The Ecological Significance of the Herbaceous Layer in Temperate Forest Ecosystems. BioScience
2007
,57, 845–858.
[CrossRef]
29. ForstBW. Jahresbericht 2012 des Landesbetriebes ForstBW; ForstBW: Baden-Württemberg, Germany, 2012; p. 58.
30.
Langer, G.; Bressem, U. Eschentriebsterben—Praxisinformation Nr. 4; Bayerische Landesanstalt für Wald und Forstwirtschaft:
Göttingen, Germany, 2016. Available online: https://www.lwf.bayern.de/mam/cms04/waldschutz/dateien/bonitur_von_
alteschen.pdf (accessed on 4 December 2020).
31.
Lygis, V.; Vasiliauskas, R.; Larsson, K.-H.; Stenlid, J. Wood-inhabiting fungi in stems of Fraxinus excelsior in declining ash stands
of northern Lithuania, with particular reference to Armillaria cepistipes. Scand. J. For. Res. 2005,20, 337–346. [CrossRef]
32. Geiger, R. Überarbeitete Neuausgabe von Geiger, P. Köppen-Geiger / Klima der Erde; Klett-Perthes: Gotha, Germany, 1961.
33.
Bayerische Landesanstalt für Landwirtschaft. Agrarmeteorologie by: Weather Data. (Open Document). Available online:
https://dynamax.com/images/uploads/papers/HemiView_Manual.pdf (accessed on 4 December 2020).
34.
Schwab, A.; Stammel, B.; Kiehl, K. Seed dispersal via a new watercourse in a reconnected floodplain: Differences in species
groups and seasonality. Restor. Ecol. 2018,26, S103–S113. [CrossRef]
35.
Margraf, C. Die Vegetationsentwicklung der Donauauen Zwischen Ingolstadt und Neuburg: Vegetationskundlich-ökologische Studie
über den Wandel Einer Auenlandschaft 30 Jahre Nach Staustufenbau; Hoppea, Denkschriften der Regensburgischen Botanischen
Gesellschaft: Regensburg, Germany, 2004.
Forests 2021,12, 128 12 of 12
36.
Lang, P.; Ewald, J. Predictive modelling and monitoring of Ellenberg moisture value validates restoration success in floodplain
forests. Appl. Veg. Sci. 2014,17, 543–555. [CrossRef]
37.
Doben, K.; Doppler, G.; Freudenberger, W.; Jerz, H.; Meyer, R.K.F.; Mielke, H.; Ott, W.-D.; Rohrmüller, J.; Schmidt-Kaler, H.;
Schwerd, K.; et al. Geologische Karte von Bayern; 4. Auflage; Bayerisches Geologisches Landesamt: Munich, Germany, 1996.
38.
Lenz, H.; Straßner, L.; Baumann, M.; Baier, U. Boniturschlüssel zur Einstufung der Vitalität von Alteschen. Afz-Der Wald
2012
,3,
18–129.
39. Londo, G. The decimal scale for releves of permanent quadrats. Vegetatio 1976,33, 61–64. [CrossRef]
40.
Ellenberg, H.; Weber, H.E.; Düll, R.; Wirth, V.; Werner, W.; Paulißen, D. (Eds.) Zeigerwerte von Pflanzen in Mitteleuropa; 2. Auflage;
Verlag Erich Goltze GmbH & Co. KG: Göttingen, Germany, 1992.
41. Monteith, J.L. Principles of Environmental Physics; Reprinted with corr.; Arnold: London, UK, 1973; ISBN 0713123753.
42.
Delta-T Devices. User Manual for HemiView, Version 2.1. 1999. Available online: https://dynamax.com/images/uploads/
papers/HemiView_Manual.pdf (accessed on 4 December 2020).
43.
Welles, J.M.; Norman, J.M. Instrument for Indirect Measurement of Canopy Architecture. Agron. J.
1991
,83, 818–825. [CrossRef]
44.
Marigo, G.; Peltier, J.-P.; Girel, J.; Pautou, G. Success in the demographic expansion of Fraxinus excelsior L. Trees
2000
,15, 1–13.
[CrossRef]
45.
Welles, J.M.; Cohen, S. Canopy structure measurement by gap fraction analysis using commercial instrumentation. J. Exp. Bot.
1996,47, 1335–1342. [CrossRef]
46.
Mölder, A.; Bernhardt-Römermann, M.; Schmidt, W. Herb-layer diversity in deciduous forests: Raised by tree richness or beaten
by beech? For. Ecol. Manag. 2008,256, 272–281. [CrossRef]
47. Thomas, P.A. Biological Flora of the British Isles: Fraxinus excelsior. J. Ecol. 2016,104, 1158–1209. [CrossRef]
48.
Kerr, G.; Cahalan, C. A review of site factors affecting the early growth of ash (Fraxinus excelsior L.). For. Ecol. Manag.
2004
,188,
225–234. [CrossRef]
49.
Wagner, S. Ein Modell zur Fruchtausbreitung der Esche (Fraxinus excelsior L.) unter Berücksichtigung von Richtungseffekten.
Allg. Forst Jagdztg. 1997,168, 149–155.
50. BMEL. The Forests in Germany—Selected Results of the Third National Forest Inventory; BMEL: Bonn, Germany, 2014.
51.
Gilliam, F.S. Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J. Ecol.
2006
,94, 1176–1191.
[CrossRef]
52.
Plue, J.; van Gils, B.; de Schrijver, A.; Peppler-Lisbach, C.; Verheyen, K.; Hermy, M. Forest herb layer response to long-term light
deficit along a forest developmental series. Acta Oecol. 2013,53, 63–72. [CrossRef]
53.
Lyon, J.; Sharpe, W.E. Impacts of Hay-Scented Fern on Nutrition of Northern Red Oak Seedlings. J. Plant Nutr.
2003
,26, 487–502.
[CrossRef]
54.
Oijen, D.; Feijen, M.; Hommel, P.; Ouden, J.; Waal, R. Effects of tree species composition on within-forest distribution of
understorey species. Appl. Veg. Sci. 2005,8, 155–166. [CrossRef]
55.
Langenbruch, C.; Helfrich, M.; Flessa, H. Effects of beech (Fagus sylvatica), ash (Fraxinus excelsior) and lime (Tilia spec.) on soil
chemical properties in a mixed deciduous forest. Plant Soil 2012,352, 389–403. [CrossRef]
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