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Forest Ecology and Management 330 (2014) 228–239 Contents lists available at ScienceDirect Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco 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). 236 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. References AG Geobotanik, 2013. Gemeinsame Datenbank der AG Geobotanik in SchleswigHolstein und Hamburg e. V. und des Landesamtes für Landwirtschaft, Umwelt und ländliche Räume des Landes Schleswig-Holstein. Kiel and Flintbek. Arnold, V., 2011. 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