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Forest Ecology and Management 330 (2014) 228–239
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Forest Ecology and Management
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Determining ancient woodland indicator plants for practical use:
A new approach developed in northwest Germany
Marcus Schmidt a, Andreas Mölder a,⇑, Egbert Schönfelder a, Falko Engel a, Inga Schmiedel b,
Heike Culmsee c
a
Northwest German Forest Research Station, Department A (Forest Growth), Section Forest Conservation and Natural Forest Research, Grätzelstraße 2, D-37079 Göttingen, Germany
Georg-August University Göttingen, Albrecht von Haller Institute for Plant Sciences, Department Vegetation and Phytodiversity Analysis, Untere Karspüle 2, D-37073 Göttingen,
Germany
c
DBU Natural Heritage, German Federal Foundation for the Environment, An der Bornau 2, D-49090 Osnabrück, Germany
b
a r t i c l e
i n f o
Article history:
Received 24 April 2014
Received in revised form 26 June 2014
Accepted 27 June 2014
Keywords:
Floristic datasets
Forest species
Historical maps
Nature conservation
Recent woodland
Habitat continuity
a b s t r a c t
Ancient woodlands that have been in continuous existence for hundreds of years have a floristic
composition which greatly differs from younger afforestations. The occurrence of certain associated
vascular plant species, termed ‘‘ancient woodland indicator plants‘‘, can be used to recognise the continuity
of woodland cover. Ancient woodland habitats frequently contain a typical and rich forest biodiversity
and can often be regarded as ‘‘biodiversity hotspots’’. To pinpoint these habitats for nature conservation,
there is a need to compile ancient woodland indicator lists with a widespread validity.
In this study, we introduce a new methodical approach that enables the compilation of such lists from
the readily available resources of plant species monitoring programs, archive records, and land cover
data. Using northwest Germany as a model region, we have developed an ecologically grounded list of
67 ancient woodland indicator plants for this area. In this context, we consider the ‘‘ancient woodland
indicator plants’’ as a subset of the larger group of ‘‘ancient woodland plants’’.
The widely applicable ancient woodland indicator plants list presented here may be a useful tool for
future forest nature conservation. Potential applications include: (a) the identification of ancient
woodlands in areas where historical maps are lacking, (b) the identification of biodiversity hotspots of
ancient woodland indicator plants, and (c) locating ancient semi-natural woodlands.
Finally, we highlight the importance of effective conservation management, which should seek to
promote the typical plant diversity of ancient semi-natural woodlands. In doing so, conservation
management should promote the preservation of remaining ancient deciduous woodlands and inhibit
the conversion of ancient woodlands to coniferous or mixed forests.
Additionally, conservation management should strengthen the connections between recent and ancient
woodlands through habitat corridors. Furthermore, careful forest management of deciduous ancient
woodland sites with high typical woodland plant diversity has to be ensured to avoid soil damage.
Ó 2014 Elsevier B.V. All rights reserved.
1. Introduction
The continuity of woodland cover in time is regarded as a key
factor for biodiversity in temperate forest ecosystems (Peterken,
1974; Singleton et al., 2001; Hermy and Verheyen, 2007; Moning
and Müller, 2009; Nascimbene et al., 2013). Numerous studies
have shown that woodlands in existence for hundreds of years
differed greatly from younger afforestations with regard to their
floristic composition (Wulf, 2003; Ito et al., 2004; Hermy and
⇑ Corresponding author. Tel.: +49 551 69 401 313; fax: +49 551 69 401 160.
E-mail address: [email protected] (A. Mölder).
http://dx.doi.org/10.1016/j.foreco.2014.06.043
0378-1127/Ó 2014 Elsevier B.V. All rights reserved.
Verheyen, 2007; Svenning et al., 2008; Kelemen et al., 2014). This
discrepancy is particularly distinctive in regions with a low
proportion of woodland cover and a high degree of fragmentation
(Ferris and Humphrey, 1999; Hermy et al., 1999; Wulf, 2003). In
contrast, the linkage between woodland continuity and the
occurrence patterns of woodland plant species is lower in areas
where the majority of woodland is ancient and features a smaller
degree of ecological isolation (Dzwonko and Gawroński, 1994;
Ferris and Humphrey, 1999; Schmidt et al., 2009).
In Great Britain, the term ‘ancient woodland’ defines land that
has been continuously wooded since at least 1600 AD (Spencer
and Kirby, 1992; Goldberg et al., 2007; Stone and Williamson,
2013). In our study, with a focus on the highly fragmented ancient
M. Schmidt et al. / Forest Ecology and Management 330 (2014) 228–239
woodland of northwest Germany, we refer to ‘ancient woodland’ as
land that has been continuously wooded since at least 1800 AD,
since only from this point on are area-wide coverage data on
historically old woodland sites available (Wulf, 2003; Glaser and
Hauke, 2004). Ancient woodlands with a long habitat continuity
harbour a high number of rare and threatened species, and are
therefore of particular importance for nature conservation (Rose,
1999; Rackham, 2003; Hermy and Verheyen, 2007; Leuschner
et al., 2014).
Based on 22 regional studies from northwest and Central
Europe, Hermy et al. (1999) compiled a list of 132 vascular plants
closely linked to ancient woodland. Verheyen et al. (2003)
evaluated 20 field studies from eight European countries and four
northeast American states that compared the vegetation of ancient
and recent forests. From these they concluded that the response of
forest plant species to land use coincided with a clustering of
species featuring different ecological characteristics. In regard to
this, slowly colonising species, many of which occur in ancient
forests, are typically characterised by low dispersibility
(Verheyen et al., 2003; Kimberley et al., 2013).
The continuity of woodland cover can be recognised by means
of certain associated vascular plant species, known as ‘‘ancient
woodland indicator plants’’ (Rose, 1999; Glaves et al., 2009). In
Great Britain, several regionalised lists of ancient woodland
indicator plants have been compiled over the last 30 years (Rose,
1999; Glaves et al., 2009), initiated by the work of Peterken (1974).
In this study, we consider the ‘‘ancient woodland indicator plants’’
as a subset of the larger group of ‘‘ancient woodland vascular
plants’’, even though there is no clear differentiation in literature.
Ancient woodland habitats frequently contain a typical and rich
forest biodiversity and can often be regarded as ‘‘biodiversity
hotspots’’. Ancient woodland indicators are an important tool to
determine these valuable habitats (Myers et al., 2000; Hermy
and Verheyen, 2007; Meyer et al., 2009; Mölder et al., 2014a).
Furthermore, the occurrence of ancient woodland indicator plants
can be an indicator for the conservation value of adjacent open
areas. In this regard, Diekmann et al. (2008) pointed out that forest
and open-habitat specialists respond not only similarly to
landscape heterogeneity and environmental gradients, but also to
regional patterns of land use and habitat continuity.
According to Hermy et al. (1999), due to the distinct local
variation in the ecological behaviour of forest plant species, regional
lists of ancient woodland indicator plants are more appropriate
than one Pan-European list. This point of view has been supported
by numerous other authors (e.g., Rose, 1999; Wulf, 2004; Glaves
et al., 2009; Perrin and Daly, 2010). However, for the application
of ancient woodland indicator lists (e.g., by nature conservation
authorities or woodland surveyors), it is more convenient to cover
larger areas at the supra-regional greater landscape level in
order to achieve enhanced validity and comparability. Here, we
present a new methodological approach for the identification of
supra-regionally implementable ancient woodland indicator
plants. In contrast to previous studies, we have not adopted our
ancient woodland indicator plant list from a number of previous
single studies or local observations. Instead, we systematically
evaluated plant distribution data of floristic surveys in relation to
ancient woodland cover data from state-wide inventories. In doing
so, we determined ancient woodland indicators using consistent
and repeatable statistical methods. We have used the large area
of northwest Germany as a model region. Here, in these Pleistocene
lowlands, ancient woodlands are scattered and their extent is
relatively low (Glaser and Hauke, 2004). We would therefore expect
a strong association of certain woodland plant species with these
woodlands. In addition, the study area is covered by a mapping
program of the distribution of vascular plants with a resolution
of ca. 30 km2 and so provides a promisingly large data set.
229
In developing the ancient woodland indicator plant method, we
addressed the following questions:
(1) Which forest plant species can be classified as supraregionally valid ancient woodland plants for the area of
northwest Germany?
(2) Are there groups of ancient woodland plants that are related
to certain environmental conditions of different woodland
types?
(3) Which of the ancient woodland plants are suitable indicators
for application in forestry and nature conservation practice?
2. Materials and Methods
2.1. Study area
The study was conducted in northwest Germany and covered
the entire federal states of Schleswig–Holstein and Bremen and
the lowland parts of the state of Lower Saxony (altogether covering
a total area of 53,549 km2). We delimitated the borderline between
the lowland and the upland parts of Lower Saxony by following
Garve et al. (2007). Based on the German network of topographical
maps (scale 1:25,000), the study area was divided into a grid
of 2378 quadrants, of which each grid cell had a resolution of
approximately 5.5 5.5 km or 30 km2 (Fig. 1).
In the Pleistocene lowlands of northwest Germany, natural
woodlands would be dominated by deciduous tree species,
especially beech (Fagus sylvatica). However, as elsewhere in Central
Europe, there are no remaining woodlands completely unaffected
by long-term human activity (Szabó, 2009; Ellenberg and
Leuschner, 2010; Arnold, 2011). The middle of the 18th century
saw initial attempts to establish conifer plantations on infertile
heathlands; a century later, for the first time, coniferous and mixed
forests (consisting of broadleaved and coniferous trees) reached
significant proportions (Niemann, 1809; Kremser, 1990; Hase,
1997). Since then, even deciduous stands on ancient woodland
sites have been converted to conifer plantations or mixed forests
(see Table 1; ‘‘coniferous ancient woodland’’ or ’’mixed ancient
woodland’’). This is especially true for nutrient-poor sites (Glaser
and Hauke, 2004). Currently, 26% of the woodlands in our study
area are ancient. The proportion of deciduous ancient woodland
amounts to 7%. In contrast to other European regions (e.g., parts
of Great Britain), coppicing played only a minor role in northwest
German ancient woodlands during the last 200 years (Kremser,
1990; Hase, 1997; Rackham, 2003).
2.2. Data sets
The floristic data for Lower Saxony and Bremen were obtained
from the database of the Lower Saxon plant species monitoring
program (NLWKN 1982–2003; Garve et al., 2007). For Schleswig–
Holstein, floristic data was collected by Raabe (1987) and the AG
Geobotanik (2013) from 1961 to 2012. From these data sets, we
considered the 452 vascular plant species that are closely bound
to forest habitats according to the German Forest Vascular Plant
Species List (Schmidt et al., 2011). 164 species belong to category
1.1 (largely restricted to closed forests), 38 species to category
1.2 (preferring forest edges and clearings), and 250 species to
category 2.1 (occurring in forests, as well as in open habitats).
For each of these plant species, we ascertained the occurrence
(presence or absence) in each topographic map quadrant.
Nomenclature followed Wisskirchen and Haeupler (1998).
We determined the ancient woodland area (area_aw) and
proportion (perc_aw) in each quadrant, distinguishing respectively
between ancient woodland sites currently dominated by
deciduous tree species (perc_daw), coniferous tree species
230
M. Schmidt et al. / Forest Ecology and Management 330 (2014) 228–239
Fig. 1. The study area of northwest Germany, including the entire states of Bremen and Schleswig–Holstein and the lowlands of the state of Lower Saxony. The displayed
2378 grid cells are the basic units for the vascular plant survey programs.
Table 1
Woodland area and proportions of recent and ancient woodlands in the study area of northwest Germany.
Woodland type
Total woodland area
Recent woodland (younger than ca. 200 years)
Ancient woodland (older than ca. 200 years)
Deciduous ancient woodland
Mixed ancient woodland
Coniferous ancient woodland
Variables
Area (ha)
Proportion (%)
aw
daw
maw
caw
829,252
612,817
216,435
61,657
67,915
86,863
100
73.9
26.1
7.4
8.2
10.5
(perc_caw) and a mixture of both types (perc_maw) (Table 1). For
Schleswig–Holstein, data on ancient woodland was obtained from
Glaser and Hauke (2004), and for Lower Saxony and Bremen we
used high-resolution data provided by the Lower Saxon forest
planning agency. Both data sources utilised historical land survey
maps (compiled mostly between 1750 and 1800) and younger
topographical maps in order to determine whether current woodland
has been continuously wooded since 1800 or not. Woodland with
forest continuity since at least 1800 was regarded as ancient (Wulf,
2003; Glaser and Hauke, 2004), and information on current tree
species composition has been derived from forest inventories.
All spatial data was processed in QGIS (v. 2.2; QGIS
Development Team, 2014). We removed 671 quadrants (grid cells)
without forest cover and/or plant species occurrence from the data
set, thus the combined data on plant species and woodland
distributions for 1707 quadrants were used in the final analysis.
2.3. Statistical analysis
2.3.1. Identification of supra-regional ancient woodland plants
Based on a sequential matrix (M1, in which each row describes
the occurrence of a species in an arbitrary quadrant), we computed
an incidence matrix (M2) as follows:
M2 ¼ ½mi;j ;
ð1Þ
where i is equal to quadrants 1–1707, and j is equal to species
1–452, with mi,j either having the value 0 or 1 (binary values).
M. Schmidt et al. / Forest Ecology and Management 330 (2014) 228–239
Another
matrix
M3,
contained
data
on
the
five
ancient
woodland
variables
for
each
quadrant
(perc_aw, perc_daw, perc_maw, perc_caw, area_aw; Table 1),
either expressed in hectares (_area) or as a percentage (_perc).
Both matrices M2 and M3 were joined, on the basis of the unique
number of the quadrants, to generate matrix M4. Based on matrix
M4, for each combination [species * ancient woodland variable] a
generalised linear model (GLM) for binary data (Fahrmeir et al.,
2009) was computed. If a species was present in less than 0.5% of
all quadrants, it was excluded from further analyses due to
possible convergence difficulties. Finally, 390 of the 452 species
remained in the analysis. The most frequent species Glechoma
hederacea occurred in 99.0% of all investigated quadrants.
Therefore, no upper threshold was necessary. The resulting test
statistics for the regression parameter were used for creating
matrix M5 (displayed in a variance table, Appendix Table A.1),
in which pi,j corresponded to the test statistics zi,j of each GLM:
M5 ¼ ½pi;j ;
ð2Þ
where i is equal to species 1–390, and j is equal to ancient woodland
variables 1–5.
Since all the GLMs featured the same sample size (number of
quadrants) and the same structure, we were able to interpret the
z-values without further weighting: with regard to an ancient
woodland variable, z-values around 0 indicated no relationship,
while high z-values (>10) indicated a very close connectivity;
negative z-values indicated a connectivity to recent woodland.
This variance table was furthermore used for conducting a
principal component analysis (PCA; cf. Venables and Ripley,
2002). In the PCA, we considered five ancient woodland variables
(perc_aw, perc_daw, perc_maw, perc_caw, area_aw; Table 1). The
variable ‘‘area of ancient woodlands’’ (area_aw) in addition to the
variable ‘‘proportion of ancient woodlands’’ (perc_aw) provided
additional information on the significance of forest area for the
distribution patterns of plant species.
A biplot was created, which allowed for the analysis not only of
the correlation between the variables, but also of the relationship
between the ancient woodland variables and the species.
By the use of k-means clustering (cf. Venables and Ripley, 2002),
we grouped all species into seven clusters, which were interpretable
in a meaningful way. The number of seven clusters was confirmed
by applying the R software with the ‘‘clValid’’ package (Brock et al.,
2008). A combined presentation (biplot) of the clusters and the
(species) coordinates of the first and second PCA axis allowed for
the interpretation of relationships between cluster composition,
species occurrence and ancient woodland variables. With the
purpose of interpreting the seven clusters ecologically in our
analysis, we also included Ellenberg indicator values (EIV) for light,
reaction, nitrogen and moisture (Ellenberg et al., 2001). EIV and
z-values were tested for differences between the seven species
clusters (Kruskal Wallis H-test, p 6 0.05, with subsequent
Bonferroni-corrected Wilcoxon rank-sum test). For the few species
that were lacking particular EIV, we calculated auxiliary indicator
values by averaging over all quadrants. In order to then fit the
EIV onto the PCA plot, we used the function ‘‘envfit’’ provided by
the ‘‘vegan’’ package in R (Oksanen et al., 2012).
All statistical analyses were performed by using the R software
version 3.0.1 (R Development Core Team, 2013) with the ‘‘vegan’’
package (Oksanen et al., 2012) and the ‘‘clValid’’ package (Brock
et al., 2008). Significance of statistical tests was noted as follows:
***
= p 6 0.001; ** = p 6 0.01; * = p 6 0.05; n.s. = p > 0.05.
2.3.2. Compilation of an ancient woodland indicator plant list for
practical use
The GLM, PCA and cluster analyses served as a screening
procedure. In order to derive an ancient woodland indicator plant
231
list from the previously compiled variance table, we applied those
species groups found to be indicative of ancient woodlands to an
independent dataset. This dataset consisted of point data records
for vascular plants (1980–2013; AG Geobotanik, 2013) and a
detailed ancient woodland inventory of the Schleswig–Holstein
State Forests (Dubberke-Spandlowski, 2011). The Schleswig–Holstein
State Forests comprise 50.000 ha of woodland scattered all
over Schleswig–Holstein.
For all plant species of the aforementioned dataset reported in
more than 25 points (with the omission of extreme rarities; see
Rose, 1999), we calculated the percentage of point data records
situated on ancient woodland sites. In doing so, regions with a high
density of ancient woodland indicators could be separated from
those hosting none or only few of these species. Non-native tree
species were also excluded from this analysis. If P75% of a species’
occurrences were situated in ancient woodlands, that particular
species was then regarded as an ancient woodland indicator plant.
The 75% threshold was chosen according to the interpretation of the
Revised Index of Ecological Continuity (Coppins and Coppins, 2002).
3. Results
3.1. Identification of supra-regional ancient woodland plants
Variance analysis resulted in z-values of 390 species in
dependence of five ancient woodland variables (Appendix
Table A.1). Z-values ranged from 19.2 to 16.8 (Fig. 2). The
proportion of ancient woodland (perc_aw) was strongly determined
by the proportion of deciduous woodland on ancient woodland
sites (perc_daw), as shown by the very close correlation of the
z-values of both variables (Pearson’s r = 0.99, p-value 6 0.001). This
relationship was also obvious from the results of the PCA (Fig. 3).
Similarly, the proportion of coniferous forests on ancient woodland
sites (perc_caw) and the proportion of mixed forests on ancient
woodland sites (perc_maw) were almost congruent in PCA results
and correlation of the z-values (r = 0.84, p-value 6 0.001).
As a result of the k-means cluster analysis, the list of 390 species
was divided into seven groups (Table 2), which were each named
after a typical plant species. The seven groups were ordered according
to their preference for ancient or recent woodlands and to Ellenberg
indicator values (EIV). With respect to woodland continuity, three
groups of ancient woodland plants (A, Galium odoratum group;
B, Mercurialis perennis group; C, Oxalis acetosella group) were
distinguished from one group of recent woodland plants (G, Agrostis
capillaris group), and three further groups of more or less indifferent
species (D, Ranunculus ficaria group; E, G. hederacea group;
F, Deschampsia flexuosa group) (Fig. 4). These groups largely differed
in their z-values (Fig. 2) and in their Ellenberg light values (Fig. 4,
Table 2, correlation with the first PCA axis: r = 0.33, p-value
6 0.001). The groups showed a gradation, from the G. odoratum group
indicating darkest conditions to the A. capillaris group indicating
lightest forest floor conditions. Furthermore, the groups showed
largely varying reaction values (Fig. 4, Table 2, correlation with
the second PCA axis: r = 0.32, p-value 6 0.001), with the M. perennis,
G. odoratum, and R. ficaria groups indicating most base-rich soil
conditions. Across all groups, Ellenberg nitrogen values exerted a
minor influence and soil moisture values were not significant.
Considering z-values (Fig. 2), the G. odoratum group (A in Fig. 4,
Appendix Table A1) was most closely associated with ancient
deciduous woodland. This group was mainly characterised by
shade-tolerant plant species. Most of these are indicators of
moderately acidic to weakly basic soils (Table 2). Species of the
M. perennis group (B in Fig. 4) were also strongly connected to
deciduous ancient woodlands (Fig. 2), but the species of this
group, compared to the G. odoratum group, occurred on woodland
sites with better conditions of light and base supply (Table 2). In
Ancient woodland plants
Groups
Groups
Groups
Recent woodland plants
Groups
Galium odoratum
Mercurialis perennis
Oxalis acetosella
Ranunculus ficaria
Glechoma hederacea
Deschampsia flexuosa
Agrostis capillaris
Species number
Mean z values (perc_daw)
z values (perc_daw), SD
45
14.8
2.2
48
12.6
2.5
70
7.6
1.8
102
4.6
1.6
57
1.8
2.4
49
0.2
1.9
19
11.0
2.9
Mean EIV for light
EIV for light, SD
Galium odoratum
Mercurialis perennis
Oxalis acetosella
Ranunculus ficaria
Glechoma hederacea
Deschampsia flexuosa
Agrostis capillaris
4.3
1.6
–
n.s.
n.s.
60.001***
60.001***
60.001***
0.002**
5.2
1.7
–
–
n.s.
n.s.
n.s.
0.03*
n.s.
4.8
1.4
–
–
–
60.001***
60.001***
60.001***
0.008**
5.9
1.5
–
–
–
–
n.s.
n.s.
n.s.
6.3
1.1
–
–
–
–
–
n.s.
n.s.
6.2
1.3
–
–
–
–
–
–
n.s.
6.3
1.2
–
–
–
–
–
–
–
Mean EIV for reaction
EIV for reaction, SD
Galium odoratum
Mercurialis perennis
Oxalis acetosella
Ranunculus ficaria
Glechoma hederacea
Deschampsia flexuosa
Agrostis capillaris
6.3
1.2
–
n.s.
0.01**
n.s.
60.001***
n.s.
0.02*
7.0
1.0
–
–
60.001***
n.s.
60.001***
n.s.
60.001***
5.1
1.7
–
–
–
0.01**
n.s.
n.s.
n.s.
6.2
1.8
–
–
–
–
60.001***
n.s.
n.s.
5.6
2.1
–
–
–
–
–
n.s.
n.s.
4.3
1.8
–
–
–
–
–
n.s.
n.s.
4.3
1.5
–
–
–
–
–
–
–
Mean EIV for nitrogen
EIV for nitrogen, SD
Galium odoratum
Mercurialis perennis
Oxalis acetosella
Ranunculus ficaria
Glechoma hederacea
Deschampsia flexuosa
Agrostis capillaris
5.7
1.4
–
–
n.s.
n.s.
60.001***
n.s.
n.s.
5.8
1.6
–
–
n.s.
0.03*
60.001***
n.s.
n.s.
5.0
1.9
–
–
–
n.s.
0.03*
n.s.
n.s.
4.6
2.0
–
–
–
–
n.s.
n.s.
n.s.
4.6
2.5
–
–
–
–
–
n.s.
n.s.
3.7
2.1
–
–
–
–
–
–
n.s.
5.8
2.2
–
–
–
–
–
–
–
Mean EIV for moisture
EIV for moisture, SD
Agrostis capillaris
All other groups
6.1
1.2
0.03*
n.s.
5.7
1.3
n.s.
n.s.
5.8
1.5
n.s.
n.s.
6.5
2.2
n.s.
n.s.
6.2
2.1
n.s.
n.s.
5.4
1.9
n.s.
n.s.
4.8
0.9
–
n.s.
M. Schmidt et al. / Forest Ecology and Management 330 (2014) 228–239
Groups
Indifferent woodland plants
232
Table 2
Species numbers, mean z values of the variable ‘‘proportion of deciduous woodland on ancient woodland sites’’ (perc_daw), and Ellenberg indicator values (EIV) of the seven species groups. p values of significant differences between the
EIV of two groups are given in bold. *** = p 6 0.001; ** = p 6 0.01; * = p 6 0.05; n.s. = p > 0.05. SD = standard deviation.
M. Schmidt et al. / Forest Ecology and Management 330 (2014) 228–239
Fig. 2. Variation in z-values of the variable ‘‘proportion of deciduous woodland on
ancient woodland sites’’ (perc_daw) given for different species groups: A – Galium
odoratum group, B – Mercurialis perennis group, C – Oxalis acetosella group,
D – Ranunculus ficaria group, E – Glechoma hederacea group, F – Deschampsia
flexuosa group, G – Agrostis capillaris group. Significant differences are indicated by
different lower case letters.
contrast, species of the O. acetosella group (C in Fig. 4) differed from
the aforementioned groups concerning their ecological behaviour
and in their degree of linkage to ancient woodlands (Fig. 2). Only
233
a few species in this group reached high z-values (>10). Overall,
species of this group were less strongly linked to ancient deciduous
woodlands (Fig. 2) and also tended to occur in coniferous or mixed
ancient woodlands (Figs. 3 and 4). The respective species often
preferred medium shade and grew on acidic to weakly acidic soils
(Table 2).
The R. ficaria group (D in Fig. 4) was largely indifferent to
woodland continuity. Nevertheless, several species of this group
were characterised by comparatively high z-values in relation to
the proportion of ancient woodland and the proportion of deciduous
woodland on ancient woodland sites (Fig. 2). This showed that in
the group definition it was difficult to draw absolute limits. The
species of the R. ficaria group preferred semi-shady conditions
and grew on moderate acidic to basic soils (Table 3). The species
of the D. flexuosa group, as well as the G. hederacea group, were
both indifferent concerning habitat continuity, or even showed
higher affinity to recent woodlands. The former group (F in
Fig. 4) included medium shade tolerant plants or plants occurring
in light shade, and indicators for acidic up to moderate acidic soils
(Table 2). Species of the latter group (E in Fig. 4) preferred medium
shade conditions and moderately to weakly acidic soils (Table 3).
Finally, the A. capillaris group included recent woodland species
(G in Fig. 4), which mostly grew in locations receiving a high
amount of light and preferred acidic or moderately acidic soils
(Table 3). The species of this group were characterised by negative
z-values in relation to the proportions of ancient woodland and
deciduous woodland on ancient woodland sites (Fig. 2).
We found obvious differences in the linkage to forest habitats
between the seven plant species groups (Fig. 5). The proportion
of species that were largely restricted to closed forests (category
Fig. 3. PCA/biplot of the data listed in the variance table (Appendix Table A1). Matrix: 390 forest species (axis 1: eigenvalue = 3.31, axis 2: eigenvalue = 1.32, combined R2 of
axes 1 and 2 = 0.93). Abbreviations of the species names: see Appendix Table A1. For reasons of clarity most species names have been replaced by asterisks.
perc_aw = proportion of ancient woodlands in the total forest area per quadrant (%), perc_daw = proportion of deciduous forests on ancient woodland sites in the total forest
area per quadrant (%), perc_caw = proportion of coniferous forests on ancient woodland sites in the total forest area per quadrant (%), perc_maw = proportion of mixed forests
on ancient woodland sites in the total forest area per quadrant (%), area_aw = area of ancient woodlands in the total forest area per quadrant (ha).
234
M. Schmidt et al. / Forest Ecology and Management 330 (2014) 228–239
Table 3
List of ancient woodland indicator plants for northwest Germany. FSG = Forest species
group according to the German Forest Vascular Plant Species List (Schmidt et al.,
2011), 1.1 = largely restricted to closed forests, 1.2 = preferring forest edges and
clearings, 2.1 = occurring in forests, as well as in open habitats.
Fig. 4. PCA of the 390 forest species listed in the variance table (Appendix
Table A1). The position of the species corresponds to Fig. 3, the letters indicate the 7
groups identified by k-means clustering: A = Galium odoratum group (45 species),
B = Mercurialis perennis group (48 species), C = Oxalis acetosella group (70 species),
D = Ranunculus ficaria group (102 species), E = Glechoma hederacea group (57
species), F = Deschampsia flexuosa group (49 species), G = Agrostis capillaris
group (19 species). R = Ellenberg reaction value, N = Ellenberg nitrogen value,
L = Ellenberg light value, M = Ellenberg moisture value.
1.1) was highest in the clusters of ancient woodland species
(G. odoratum, M. perennis, and O. acetosella groups). In contrast,
indifferent species (R. ficaria, D. flexuosa, and G. hederacea groups)
and recent woodland species (A. capillaris group) grew predominantly
in forests, as well as in open areas (category 2.1). The proportion of
vascular plants largely restricted to closed forests (category 1.1)
was lowest in the A. capillaris group of recent woodland species.
In this group, however, there was a prominence of species
preferring forest edges and clearings (category 1.2).
3.2. Compilation of an implementable ancient woodland indicator
plant list
The list of ancient woodland indicator plants (Table 3; Appendix
Table A1) comprised 67 species. Most of them (85%) belonged to
the forest species category 1.1 (largely restricted to closed forests),
13% were part of the category 1.2 (preferring forest edges and
clearings), and 2% belonged to the category 2.1 (occurring in
forests, as well as in open land).
Fig. 6 displays the numbers of ancient woodland indicator plant
species (forest species categories 1.1 and 1.2) present in the grid
quadrants for northwest Germany. The highest numbers of indicator species were found in Schleswig–Holstein, where the eastern
hill country as a young moraine landscape emerges. The small
and fragmented ancient woodlands, which are predominant in this
region, are characterised by nutrient-rich soils (Niemann, 1809;
Hase, 1997). Such nutrient-rich sites support the highest diversity
of ancient woodland plant species (e.g., Wulf, 2004).
4. Discussion
No.
Species name
FSG
Woodland species group
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
Actaea spicata
Allium ursinum
Anemone ranunculoides
Arum maculatum
Blechnum spicant
Brachypodium sylvaticum
Campanula trachelium
Cardamine bulbifera
Carex pallescens
Carex remota
Carex strigosa
Carex sylvatica
Carpinus betulus
Chrysosplenium alternifolium
Chrysosplenium oppositifolium
Circaea alpina
Circaea lutetiana
Circaea x intermedia
Convallaria majalis
Corydalis cava
Crepis paludosa
Dactylorhiza fuchsii
Epipactis helleborine
Equisetum hyemale
Equisetum pratense
Equisetum sylvaticum
Equisetum telmateia
Festuca altissima
Gagea spathacea
Galium odoratum
Geum rivale
Gymnocarpium dryopteris
Hordelymus europaeus
Hypericum pulchrum
Ilex aquifolium
Impatiens noli-tangere
Lamium galeobdolon
Listera ovata
Luzula pilosa
Luzula sylvatica subsp. sylvatica
Lysimachia nemorum
Maianthemum bifolium
Melica uniflora
Mercurialis perennis
Milium effusum
Neottia nidus-avis
Orchis mascula
Oreopteris limbosperma
Oxalis acetosella
Paris quadrifolia
Phegopteris connectilis
Phyteuma spicatum
Platanthera chlorantha
Potentilla sterilis
Primula elatior
Pulmonaria obscura
Ranunculus auricomus agg.
Ranunculus lanuginosus
Rumex sanguineus
Sanicula europaea
Scrophularia nodosa
Scutellaria galericulata
Stachys sylvatica
Ulmus laevis
Veronica montana
Viola reichenbachiana
Viola riviniana
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
2.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
2.1
2.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
2.1
1.1
1.1
2.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
1.1
2.1
1.1
1.1
1.1
1.1
1.1
1.1
1.2
1.1
1.1
2.1
1.1
1.1
1.1
2.1
2.1
1.1
1.1
1.1
1.1
1.1
Mercurialis perennis group
Oxalis acetosella group
Mercurialis perennis group
Galium odoratum group
Oxalis acetosella group
Galium odoratum group
Mercurialis perennis group
Mercurialis perennis group
Galium odoratum group
Galium odoratum group
Mercurialis perennis group
Galium odoratum group
Oxalis acetosella group
Galium odoratum group
Galium odoratum group
Oxalis acetosella group
Galium odoratum group
Oxalis acetosella group
Oxalis acetosella group
Mercurialis perennis group
Galium odoratum group
Mercurialis perennis group
Oxalis acetosella group
Galium odoratum group
Galium odoratum group
Galium odoratum group
Mercurialis perennis group
Galium odoratum group
Galium odoratum group
Galium odoratum group
Mercurialis perennis group
Oxalis acetosella group
Mercurialis perennis group
Oxalis acetosella group
Oxalis acetosella group
Galium odoratum group
Galium odoratum group
Mercurialis perennis group
Galium odoratum group
Mercurialis perennis group
Galium odoratum group
Oxalis acetosella group
Galium odoratum group
Mercurialis perennis group
Galium odoratum group
Galium odoratum group
Mercurialis perennis group
Oxalis acetosella group
Oxalis acetosella group
Galium odoratum group
Oxalis acetosella group
Mercurialis perennis group
Galium odoratum group
Mercurialis perennis group
Galium odoratum group
Galium odoratum group
Galium odoratum group
Mercurialis perennis group
Galium odoratum group
Galium odoratum group
Oxalis acetosella group
Oxalis acetosella group
Galium odoratum group
Oxalis acetosella group
Galium odoratum group
Galium odoratum group
Galium odoratum group
4.1. Woodland plant species groups and their ecological characteristics
Of the seven woodland plant species groups identified for our
study area, we found three main groups of ancient woodland
species; the G. odoratum, M. perennis, and O. acetosella groups.
The species composition of these groups is substantially in line
with the results of other studies conducted in temperate Western
M. Schmidt et al. / Forest Ecology and Management 330 (2014) 228–239
235
Fig. 5. Linkage to forest habitats within the seven plant groups identified by k-means clustering. 1.1 – largely restricted to closed forests, 1.2 – preferring forest edges and
clearings, 2.1 – occurring in forests, as well as in open areas.
Fig. 6. Number of ancient woodland indicator plant species per topographic map quadrant in northwest Germany considering only forest species of categories 1.1 (largely
restricted to closed forests) and 1.2 (preferring forest edges and clearings).
and Central Europe (e. g., Wulf, 1997, 2004; Hermy et al., 1999;
Verheyen et al., 2003). Of particular note is the G. odoratum group,
where 71% of the plant species we recorded are also listed by
Hermy et al. (1999) as ancient forest species. In the M. perennis
group, this is true for 62% of the species and in the O. acetosella
group for only 41% of the species. On the one hand, the relatively
low concordance of the latter group may possibly be explained
by the low number of studies examining ancient woodland plants
on acidic soils (see Heinken, 1998; Matuszkiewicz et al., 2013).
Thus, Hermy et al. (1999), whose study was dependent on the
availability of local ancient woodland plant species lists, could only
draw conclusions for a locally limited species pool. On the other
hand, considering z-values, the affinity of acidophytic plant species
characterising this group to deciduous ancient woodland sites
seems to be generally less pronounced. This may be related to
the ability of many of these species to grow in coniferous or mixed
forests or, alternatively, to persist in extensively managed open
habitats (forest affinity category 2.1; Schmidt et al., 2011) such
as heathlands composed of dwarf shrubs or matt-grass swards
(Wulf, 2004; Ellenberg and Leuschner, 2010).
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M. Schmidt et al. / Forest Ecology and Management 330 (2014) 228–239
Our analysis further revealed that, even among the plants
strictly bound to forests, there is a group of species strictly linked
to recent woodlands. However, this group, the A. capillaris group, is
relatively small and includes only common and very common
species. Furthermore, we assume that a larger number of plants
linked to recent woodlands is contained in the disregarded group
of plants that may occur in forests, but preferably grow in open
areas (forest affinity category 2.2; Schmidt et al., 2011). Similar
results were found for the Prignitz region, which adjoins our study
area to the east (Wulf, 2004).
However, most of the forest plants included in our analysis
belong to one of the three groups of species that are more or less
indifferent to woodland continuity (i.e. the R. ficaria, G. hederacea,
and D. flexuosa groups). These groups contain very common and
ubiquitous forest plant species without any linkage to ancient
woodlands. Furthermore, there are many very rare species
included, whose possible (local or regional) linkage to ancient
woodlands could not be statistically verified on the supra-regional
scale of our study.
The results of the k-means cluster analysis allowed for a
reasoned interpretation of the ecological conditions with which the
species groups are linked based on mean Ellenberg indicator values
(EIV). The gradient from ancient to recent woodland species groups
corresponded particularly positively to an increase in the EIV for
light. We conclude that the light demand of plant species plays a
crucial role for their linkage to ancient or recent woodland sites
(see also Petersen, 1994; Howard and Lee, 2003). Shade-tolerant
forest species mostly belonged to one of the three groups identified
as ancient woodland species. This is also reflected by the high
proportion of plant species restricted to closed forests. In contrast,
both the species group linked to recent woodland sites and the
three groups of species more or less indifferent to woodland
continuity are characterised by a high light demand and they
contain only a few species that are restricted to closed forests.
Our results are very much in line with those of Hermy et al. (1999)
and Wulf (2004), who concluded that vascular plants characteristic
for ancient deciduous woodlands are more shade-tolerant than
other forest plant species. However, British ancient woodlands
are often characterised by more light-demanding woodland plants
due to the long history of coppicing (Kirby, 1990; Rose, 1999).
The results of the EIV for soil reaction, which are correlated to
the second axis of the PCA, require a more complex ecological
interpretation. The species with the highest demand for base
supply occur in the M. perennis group, followed by the G. odoratum
group. Both groups are highly correlated to deciduous woodland
on ancient woodland sites (as indicated by high z-values). In
contrast, the O. acetosella group (i.e. the third group of ancient
woodland species) and the three groups with more or less indifferent
woodland continuity all show a wide range of EIV for soil reaction.
Finally, the A. capillaris group of recent woodland species is
characterised by both a low need for base saturation and a narrow
range of EIV for soil reaction. From the latter, we conclude that
afforestation and recent natural forest development in our study
area occurred particularly on sites with acidic soils (cf. Kremser,
1990; Hase, 1997). Hermy et al. (1999) found that ancient
woodland plants, when compared to other forest plants, mostly
occur in woodlands with both intermediate pH values and nitrogen
availability, and are in most cases lacking on both dry and wet
sites. We could confirm their results in respect to base saturation,
but not in respect to nitrogen supply (as quantified by the EIV)
where we found only a very weak relationship to the groups of
ancient woodland species. Although for soil moisture, we found
almost no relationship, there was a distinct set of indicator species
for wet soil conditions, such as Chrysosplenium oppositifolium,
Crepis paludosa or Equisetum telmateia, which were closely linked
to ancient woodland sites, and Convallaria majalis, Orchis mascula
and Viola riviniana, a set of ancient woodland plants known to be
found on drier sites (Ellenberg et al., 2001).
4.2. A new approach in determining ancient woodland indicator plant
lists and their potential application
In Europe, lists of ancient woodland indicator plants have up
until now almost exclusively been compiled by expert knowledge
or were based on vegetation relevés in combination with local or
regional species lists (Hermy et al., 1999; Verheyen et al., 2003;
Perrin and Daly, 2010). Such lists have also been compiled for
some smaller areas of northwest Germany (Wulf, 2004). As an
expectable consequence of this approach, regional differences in
the linkage of plant species to ancient woodlands were strongly
emphasised (Wulf, 1997; Kühn, 2000). Therefore, there has been
a need to develop a more robust and standardised approach to
compile lists of ancient woodland indicator plants (Glaves et al.,
2009), which are implementable on a supra-regional scale. We
have applied a new approach by using repeatable statistical
methods and large comprehensive species distribution data sets
in combination with archive records on ancient woodlands for
the determination of ancient woodland indicator plant lists. In
doing so, we have used additional information on the ecology of
the plant species. Firstly, we reduced the list to the set of plant
species most closely linked to woodland habitats based on
information available for all of Germany and perhaps beyond
(Schmidt et al., 2011), and, secondly, we considered the preference
of the forest plant species for deciduous, coniferous, or mixed
woodland on ancient woodland sites. However, when considering
the z-values, it becomes obvious that there are no absolute limits
for the classification of a plant species as an ancient woodland indicator. There is a rather continuous transition from species closely
linked to ancient woodland sites to species with a linkage to recent
woodland sites. Hence, we developed the procedure described in
chapter 2.3.2 and compiled an implementable ancient woodland
indicator plant list. This resulted in a list of 67 significant ancient
woodland indicator plants with supra-regional validity and applicability. We believe that our approach is easily applicable to other
large areas in Europe, because high-resolution data on historical
and recent land cover and the distribution of vascular plant species
are becoming increasingly available in more and more countries
(see Table 6 in Culmsee et al., 2014). However, it has to be considered that there are not any vascular plants that grow exclusively on
ancient woodland sites (Rose, 1999; Glaves et al., 2009). In order to
identify an ancient woodland site with high accuracy, one has to
detect multiple ancient woodland indicator plants (Rose, 1999;
Kühn, 2000; Schmidt et al., 2009). With regard to the necessary
number of ancient woodland indicator plant species, the values
in the literature range from 2 (Kühn, 2000) to 27 (Honnay et al.,
1998). Honnay et al. (1998) stressed that the indicative value of
ancient woodland plant species is scale dependent. Further
research is needed in this area.
Widely applicable ancient woodland indicator plant lists
may be a useful tool for nature conservation practice, where the
potential applications are:
(a) Identification of ancient woodlands in areas where historical
maps are lacking
There are regions where historical maps are completely lacking
or where it is difficult to obtain them from archives (Rose, 1999;
Crawford, 2009). For instance, the German-wide ancient woodland
inventory provided by Glaser and Hauke (2004) does not cover the
German federal state of Hamburg as a part of northwest Germany.
For this area, the occurrence of indicator species can give evidence
of ancient woodland sites. The same is true for the region of
M. Schmidt et al. / Forest Ecology and Management 330 (2014) 228–239
southern Denmark adjacent to our study area. Ancient woodland
indicators may also be useful when ancient woodland inventories
are, due to small map resolution, less accurate for smaller woodland
patches or woodland fringes (Wulf, 2004; Goldberg et al., 2007;
Oheimb et al., 2007). In addition, ancient woodland indicators are
important for the identification of ‘‘ancient hedges’’, which are
remnants of, or were once adjacent to, original forests (Pollard
et al., 1974; Stone and Williamson, 2013). Such old linear landscape
structures can serve as propagule sources for the spread of ancient
woodland species into adjacent recent woodlands (Corbit et al.,
1999; Liira and Paal, 2013; Stone and Williamson, 2013).
(b) Identification of biodiversity hotspots of ancient woodland
indicator plants
Not every ancient woodland site shows a high species richness
in ancient woodland indicator plants. In fact, there may be a large
variation in alpha diversity due to land-use history, silvicultural
treatment, tree species composition, and nutrient supply
(Dupouey et al., 2002; Härdtle et al., 2003; Mölder et al., 2014b).
Following the ‘‘hotspot strategy’’ of Meyer et al. (2009), woodland
patches with a high diversity of ancient woodland indicator plants
should be identified and protected or managed for nature
conservation (Schmiedel et al., 2013).
(c) Ancient woodland indicator plants as indicators for ancient
semi-natural woodlands
Since ancient woodland indicator plants allow for the detection
of woodland sites with long habitat continuity, under certain
conditions, they can also serve as indicators for ancient semi-natural
woodland and natural diversity (Rose, 1999; Nordén and
Appelqvist, 2001; D’Amato et al., 2009). Habitat continuity, when
accompanied by structural continuity (e. g., the occurrence of
ancient trees), allows for conclusions to be drawn on the whole
community of woodland species including bryophytes, lichens,
fungi, or beetles (Ferris and Humphrey, 1999; Grove, 2002;
Kriebitzsch et al., 2013; Mölder et al., 2014a). In this context,
ancient woodland indicators can be part of a mapping procedure
for the identification of ancient semi-natural woodland; especially,
when historical maps are difficult to obtain (Rose, 1999; Nordén
and Appelqvist, 2001; Crawford, 2009; Goldberg et al., 2007).
5. Conclusions
In our opinion, for nature conservation practice, there is a great
need for ancient woodland indicator plant lists with supra-regional
applicability. In this study, we introduce a new methodical
approach that allows the compilation of such lists by using readily
available resources of plant species monitoring programs and land
cover data. Using the area of northwest Germany as a model
region, we presented an ecologically grounded ancient woodland
indicator plant list. In northwest Germany, where only 26% of the
woodlands are ancient, the proportion of deciduous ancient
woodland sites amounts to merely 7% and these woodlands are
highly fragmented. In such scarcely wooded, agriculturally
dominated landscapes, the value of forest islands for nature
conservation depends on historical ecological continuity (Thomas
et al., 1997). Under such circumstances, deciduous ancient woodland
sites can be hotspots of forest plant biodiversity. Furthermore, they
can act as propagule sources for the spread of ancient woodland
species into adjacent recent woodlands. However, in Europe, the
time for such a spread takes up to 350–800 years (Falinski, 1986;
Peterken, 1977; Rackham, 2003).
In order to promote the typical plant diversity of ancient
semi-natural woodlands, effective conservation management
237
should strongly support the preservation of ancient deciduous
woodlands and inhibit their conversion to coniferous or mixed
stands. The connection of recent and ancient woodlands by habitat
corridors should be strengthened (Hermy et al., 1999; De Frenne
et al., 2011; Kriebitzsch et al., 2013; Verstraeten et al., 2013;
Leuschner et al., 2014). In fragmented landscapes with intense
agriculture, no-spray buffer zones of at least 5 m should be
adopted to protect the majority of woodland species from the
impacts of agrochemicals applied to adjacent land (Gove et al.,
2007). Furthermore, the forest management of deciduous ancient
woodland sites with a high typical woodland plant diversity has
to be carefully conducted to avoid soil damage (Worrell and
Hampson, 1997; Godefroid and Koedam, 2004). These actions must
be taken in stands within protected areas (Thomas et al., 1997;
Schmiedel et al., 2013), but should also be promoted beyond, since
existing protected area networks usually cover only part of the
ecologically valuable ancient woodlands in which forest floor
diversity is particularly difficult to restore (Thompson et al.,
2003; Thomas et al., 1997; De Frenne et al., 2011).
Acknowledgments
This study was made possible by innumerable volunteers and
professionals who reported plant species occurrences in the states
of Lower Saxony, Bremen and Schleswig-Holstein. We thank
Annemarie Schacherer (Lower Saxony Water Management, Coastal
Defence and Nature Conservation Agency) and Katrin Romahn
(AG Geobotanik in Schleswig-Holstein und Hamburg e. V.) for
providing floristic data. We gratefully acknowledge the funding of
the projects ‘‘Identification of indicator species groups of grassland
and forest habitats for biodiversity monitoring and evaluation’’
(Grant Number DBU 26752) and ‘‘Identification and protection of
forest stands of special importance for biodiversity conservation’’
(Grant Number DBU 29677) by the German Federal Foundation
for the Environment (DBU). We thank Ruth Gilbert and Bob Larkin
for proofreading. We are also indebted to two anonymous
reviewers for suggestions that have greatly improved the paper.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.foreco.2014.06.
043.
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