Corresponding author: Tibor Standovár ( email@example.com )
Academic editor: Klaus Henle
© 2017 Tibor Standovár, Soma Horváth, Réka Aszalós.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Standovár T, Horváth S, Aszalós R (2017) Temporal changes in vegetation of a virgin beech woodland remnant: stand-scale stability with intensive fine-scale dynamics governed by stand dynamic events. Nature Conservation 17: 35-56. https://doi.org/10.3897/natureconservation.17.12251
The aim of this resurvey study is to check if herbaceous vegetation on the forest floor exhibits overall stability at the stand-scale in spite of intensive dynamics at the scale of individual plots and stand dynamic events (driven by natural fine scale canopy gap dynamics). In 1996, we sampled a 1.5 ha patch using 0.25 m² plots placed along a 5 m × 5 m grid in the best remnant of central European montane beech woods in Hungary. All species in the herbaceous layer and their cover estimates were recorded. Five patches representing different stand developmental situations (SDS) were selected for resurvey. In 2013, 306 plots were resurveyed by using blocks of four 0.25 m² plots to test the effects of imperfect relocation.
We found very intensive fine-scale dynamics in the herbaceous layer with high species turnover and sharp changes in ground layer cover at the local-scale (< 1 m2). A decrease in species richness and herbaceous layer cover, as well as high species turnover, characterized the closing gaps. Colonization events and increasing species richness and herbaceous layer cover prevailed in the two newly created gaps. A pronounced decrease in the total cover, but low species turnover and survival of the majority of the closed forest specialists was detected by the resurvey at the stand-scale. The test aiming at assessing the effect of relocation showed a higher time effect than the effect of imprecise relocation.
The very intensive fine-scale dynamics of the studied beech forest are profoundly determined by natural stand dynamics. Extinction and colonisation episodes even out at the stand-scale, implying an overall compositional stability of the herbaceous vegetation at the given spatial and temporal scale. We argue that fine-scale gap dynamics, driven by natural processes or applied as a management method, can warrant the survival of many closed forest specialist species in the long-run.
Nomenclature: Flora Europaea (Tutin et al. 2010) for vascular plants; Soó 1968–1980 for syntaxa
Deciduous forest, temperate forest, resurvey, forest reserve, forest developmental stage, Fagus sylvatica, ancient forest herbs
The significance of the herbaceous layer in forest biodiversity and ecosystem functioning has been widely appreciated (
Fine-scale herbaceous layer dynamics is also often linked to stand-scale dynamics. Gap formation significantly increases solar radiation and soil moisture (
These short- and long-term changes in the herbaceous layer are most often detected by resurveys of phytosociological relevés or smaller quadrats after a few years (
In our study, we were especially interested in the dynamics of the herbaceous layer at multiple spatial scales in relation to simple stand dynamic events, such as the opening and closure of smaller and larger gaps of a primeval beech forest remnant in Hungary. The exact location of the original sampling plots surveyed in 1996 was unknown, but the sampling plots could be relocated with 1 m accuracy after 17 years.
We hypothesized that in this virgin woodland remnant: 1) fine-scale changes in the herbaceous layer are evened out at the stand-scale, where no significant changes can be detected in the species pool (low species turnover) and total cover of the herbaceous layer at this temporal and spatial scale; 2) fine-scale changes in the herbaceous layer are governed by dynamic events in the tree canopy, such as opening and closing of the canopy gaps; 3) small gap stand dynamics warrant the survival of closed forest specialist herbs at the stand-scale.
The study was carried out in Kékes Forest Reserve (63 ha), which is one of last and best remnant of central European montane beech woods in Hungary. Kékes is the highest point in Hungary (1014 m) and is situated in the Mátra Mountains, northern Hungary. The climate is relatively continental. Mean annual precipitation is around 840 mm, of which 480 mm fall during the growing season. Mean annual temperature is 5.7°C, with cold winter (-4.7°C in January) and mild summer temperatures (15.5°C in July). The bedrock is andesite and andesitic tuff. The topography is extremely steep; scree slopes are characteristic. The shallow brown forest soils are mainly covered by montane beech forest (Aconito-Fagetum Soó (1930) 1960). Mixed maple-ash-lime forest (Phyllitidi-Aceretum Moor, 1952 subcarpaticum (Dostál 1933) Soó 1957) occurs in the most humid and rocky patches of the reserve on ranker type soils (
According to historical records (
In 1996, vegetation of the herbaceous layer was systematically sampled in a 120 m × 120 m patch (approximately 1.5 ha), which was divided into 16 30 m × 30 m squares with wooden sticks as field marks in the four corners. On the 120 m × 120 m patch a grid with 5 m intervals was laid out. Altogether 576 plots with 0.25 m2 were set out on the grid (see Suppl. material
To make future assessment of stand dynamics possible, in 1997 a tree stand position map (each tree individual recorded by X and Y coordinates) was created for the 1.5 ha plot (see Suppl. material
Design of the sampling methods. In each cell of a 5 m × 5 m grid a 0.25 m² plot was sampled in 1996. Blocks of four 0.25 m² plots were resampled in the same grid in 2013.
The five stand developmental situations (SDS) were identified as follows (Table
Summary information on the five stand developmental situations (SDS) studied. For explanations of the stand developmental situations, see methods.
|SDS||Soil depth||Canopy in 1996||Canopy in 2013||Herb layer in 1996||Herb layer in 2013|
Control (C): This patch was selected because the tree canopy of the closed old beech stand was undisturbed during the study period.
One-year-old gap (1YG): This gap was formed in 2012 by the fall of two large beech trees.
Three-year-old gap (3YG): This gap was created by the fall of five trees in spring 2010.
Old beech gap (OBG): This gap was formed by the fall of a single large beech tree in the early 1990s.
Old collapse (OCO): It was opened in the early 1980s.
The 306 plots resurveyed in 2013 were selected to include both the centres and the peripheries of the five SDSs (see Suppl. material
Summary information on spatial scales and number of sampling units used in this study (SDS = stand developmental situation).
|Scale of study||Represented area||Number of plots|
|In 1996||In 2013|
|Stand||1 ha||306||306×4 = 1224|
|SDS||400 m²||5 SDS×25 = 125||5 SDS×25×4 = 500|
|Local||0.25 m²||306||306×4 = 1224|
Stand-scale: Data from all the 306 plots are lumped together to characterise the 1 ha patch.
Stand developmental situation (SDS) scale: Each SDS is represented by the joined data of 25 plots located in the centre of an individual SDS. Thus, an approximately 400 m² area is sampled (which is comparable to the size of standard phytosociological relevé) for each SDS.
Fine-scale: All the 306 plots are treated separately so changes at the 0.25 m² scale can be described. Table
For our analyses we used the following variables:
Cover of the herbaceous layer: For each plot we used the sum of estimated cover values of individual species, so > 100% values can occur. Mean cover and maximal cover were calculated from the plot data for the whole stand and for the five SDSs. For the 2013 data the overall means were used: 1224 plots (306×4) for the stand-scale, 500 plots (4×125) for the SDS-scale. Changes in the abundance of herbaceous vegetation were calculated as change in total cover. To get a better understanding of the dynamics of individual species at the stand- and SDS-scales, both net and absolute cover change were calculated.
Species richness of the herbaceous layer: The number of species was calculated for all the three spatial scales and for the two sample years. The average species number per plot was also compared.
To quantify changes that occurred during the 17 years we used the mean values of the four subsamples of 2013 data (mean species richness, mean cover of the herbaceous layer of each plot). In this way we used an equal number of plots as in 1996 for the comparisons (306 plots for stand- and fine-scale, and 125 plots for SDS-scale analyses). The relationships between stand developmental situations (SDS) and magnitude of change in species richness and total herbaceous cover were studied by using Kruskal-Wallis test (H statistics), the non-parametric analogue of classical analysis of variance (
In order to quantify the changes in a species pool the following variables were calculated, where in the case of 2013 data the average values of the four subsamples were used for all calculations:
Number of colonisation events: Individual colonisation events were detected at the fine-scale (0.25 m²). The number of colonisation events (appearance of a species) was expressed as sum (all new occurrences of all species) and mean (average number of new occurrences per plot) for each spatial scale studied.
Number of extinction events: Individual extinction events were detected at the fine-scale (0.25 m²). The number of extinction events (disappearance of a species) was expressed as sum (all disappearances of all species) and mean for each spatial scale studied.
Absolute species turnover in the herbaceous layer: Absolute turnover in species composition between successive sampling years was calculated as (E + C)/2, where E and C are the number of species extinctions and colonisations, respectively (
Relative species turnover in the herbaceous layer: Relative turnover was calculated as (E + C)/(S1 + S2) × 100%, where E and C are as above and S1 and S2 are the number of recorded species present in the two years (
Colonization and extinction events and the species turnover in the herbaceous layer were also assessed in a qualitative way. The behaviour of individual species was analysed at the stand- and SDS-scales.
When the effect of relocation was analysed, we compared the size of time effect (i.e. the difference between the 1996 value and the average value of the four 2013 subsamples) and the size of relocation effect (i.e. average of paired differences between the four subsamples) by Wilcoxon matched pair test. A one-sided alternative hypothesis was applied, i.e. higher time than relocation effect. Significant differences imply that the observed differences between two sampling times cannot be caused by the imprecise re-allocation of the subsamples only.
At the stand-scale we observed a general decrease in the abundance of herbaceous vegetation between 1996 and 2013 (Figure
Changes in total herbaceous-layer vegetation cover (%) between 1996 and 2013. Dotted lines indicate the borders of the samples representing the five stand developmental situations (C, 1YG, 3YG, OBG, OCO).
At the SDS-scale we found profound differences in the magnitude and tendency of cover change from 1996 to 2013 (Table
Total vegetation cover (%) in 1996 and 2013 in the five stand developmental situations. For explanations of the stand developmental situations, see methods.
|Mean cover in 1996 (%)||Mean cover in 2013 (%)||Max. cover in 1996 (%)||Max. cover in 2013 (%)||Max. cover change/plot in 1996 (%)|
Vegetation cover decreased considerably in infilling old gaps (OCO: -50.3%; OBG: -30.3%), whereas it increased slightly (1YG: 1.6%) and more substantially (3YG: 16.7%) in recently created gaps.
At the fine-scale, i.e. at the scale of individual plots, the largest decrease and increase in total cover was -165.7% and 62.7% respectively.
The observed changes in mean cover were obtained as the balance of positive and negative changes in individual species. Most changes were attributed to only a few species. As Table
Net and absolute cover change (%) of the ten most responsive species between 1996 and 2013.
|Species name||Stand-scale||SDS-scale (5×25 plots)|
|Net Change (%)|
|Absolute change (%)|
In 1996 and 2013 we recorded 42 and 48 species, respectively, though in the latter case a four times larger area was sampled because of the four subsamples used (306 plots×4). At the stand-scale our full sample (306 locations, two surveys) contained data from 54 species (45 herbs, 6 trees, 3 shrubs), of which 50 species occurred in the 125 plots representing the five SDSs.
In contrast to the relative stability in species richness at the stand-scale, a much more variable picture was obtained when the SDS-scale was studied. In 1996 species richness varied between 7 and 23 (Table
Changes in species richness between 1996 and 2013. Dotted lines indicate the borders of the samples representing the five stand dynamic situations (C, 1YG, 3YG, OBG, OCO).
We found significant differences between the five SDSs in changes in species richness from 1996 to 2013 (Kruskal–Wallis test results, H = 56.1961, p < 0.00001). At the fine-scale (individual 0.25 m² plots) species richness was in the range of 0-10 and 0-8 in 1996 and in 2013, respectively, with high variation among the five SDSs (Table
Species richness in 1996 and 2013 in the five stand developmental situations (SDS). For explanations of the stand developmental situations, see methods. SpNo = species number.
|SDS||Species richness in 1996||Species richness in 2013||Mean SpNo/plot in 1996||Mean SpNo/plot in 2013|
Species extinctions and colonisation occurred at all spatial scales studied during the 17 years between the two samplings. At the stand-scale there were only six species that disappeared, but all of them were present at very low frequencies and abundances in 1996. Half of the recorded 12 newly occurring species were actually present in the 576 plots sampled in 1996, but were not included in the sample (306 plots) used for the resurvey.
At the SDS-scale there were considerable differences among the individual SDS. As Table
Number of extinction and colonisation events (overall mean of the four subsamples at each plot), absolute and relative species turnover in the five stand developmental situations (SDS) based on resurvey data collected in 1996 and 2013. For explanations of the stand developmental situations, see methods.
|SDS||Extinction||Colonisation||Mean Absolute Turnover/Plot||Mean Relative turnover (%)|
Quantitative results indicate relative stability at the stand-scale and rather intensive dynamics at the SDS- and fine-scales. However, to get a better understanding of the processes, it is worth looking at what species become extinct or colonise in different situations. Special interest is devoted to closed forest specialist species (
At the stand-scale, the six species that were not included in the 2013 sample were all forest species (Chrysosplenium alternifolium, Epilobium montanum, Hordelymus europaeus, Melica uniflora, Monotropa hypopitys, Viola odorata) that occurred at very low abundances in 1996. Half of the newly colonising 12 species were forest species (Actaea spicata, Campanula rapunculoides, Epipactis helleborine, Hieracium acuminatum, Poa nemoralis and Polygonatum verticillatum) that were recorded as new because of similar chance effects since, according to our field records, they were all present in 1996 within the studied 1.5 ha stand. Among the colonisers there were two ruderal species (Tussilago farfara, Cirsium arvense) and one newly appearing adventive species (Impatiens parviflora).
At the SDS-scale it is worth comparing the list of disappearing and newly appearing species. In the OBG, most extinctions were of closed forest species (e.g. Galium odoratum, Mercurialis perennis, Viola reichenbachiana, Cardamine bulbifera) and there were only a few extinctions of gap or disturbance indicating species (Chelidonium majus, Geranium robertianum, Rubus idaeus, Urtica dioica). Colonisation events were almost exclusively due to closed forest specialist species. At the rocky OCO site the observed extinctions were mainly attributable to those species (e.g. Dryopteris filix-mas, Impatiens nolitangere, Solanum dulcamara, Urtica, dioica) that occurred with high frequencies in 1996. The low number of colonisation was due to similar species because site conditions are not favourable for most closed forest specialist herbs. On the contrary, in the control plot the species pool did not change much, despite the relatively intensive dynamics (77 extinctions, 20 colonisations). Extinctions and colonisations were both due to real closed forest specialist herbs (e.g. Cardamine bulbifera, Euphorbia amygdaloides, Galium odoratum, Mercurialis perennis). In 3YG and 1YG only a low number of extinctions were recorded, mostly due to the disappearance of forest species. The large number of colonisations in these gaps was attributable to both typical gap species and to those forest species that are able to react relatively fast to changing light conditions.
Closed forest specialist species that disappeared from individual SDS (based on data of 25 plots each) by 2013. Numbers in brackets indicate the original number of occurrence of the species in 1996. For explanations of the stand developmental situations, see methods.
|Closed forest specialist herbaceous species|
|C||Melica uniflora (1)||Cardamine bulbifera, Dryopteris filix-mas, Euphorbia amygdaloides, Galium odoratum, Mercurialis perennis, Viola reichenbachiana|
|1YG||none||Dryopteris filix-mas, Galium odoratum, Galium odoratum, Viola reichenbachiana|
|3YG||none||Galium odoratum, Mercurialis perennis,|
|OBG||Circaea lutetiana (1); Hordelymus europaeus (1); Moehringia trinervia (1); Oxalis acetosella (2); Pulmonaria obscura (1)||Cardamine bulbifera, Dryopteris filix-mas, Euphorbia amygdaloides, Galium odoratum, Mercurialis perennis, Viola reichenbachiana|
|OCO||Chrysosplenium alternifolium (1); Galium odoratum (2)||Dryopteris filix-mas, Lamiastrum galeobdolon luteum, Impatiens noli-tangere, Oxalis acetosella, Polystichum braunii|
Our results on the effects of relocation error showed that time effect was significantly higher than relocation effect both in the case of species richness (306 pairs of plots, Wilcoxon matched pair test results, T = 8475, Z = 7.769055, p < 0.00001) and in the case of total cover of the herbaceous layer (306 pairs of plots, Wilcoxon matched pair test results, T = 9932, Z = 6.983762, p < 0.00001). Consequently, differences between data from 1996 and average data of the four subsamples of 2013 cannot be merely attributable to imprecise relocation of subsamples.
After 17 years we found low species turnover and a general decrease in herbaceous cover at the stand-scale. Therefore, our first hypothesis is only partly supported. We found an overall stability of the species pool in the herbaceous layer at the stand-scale, whereas the abundance of vegetation (measured as total herb cover) changed considerably.
Several analyses pointed out that a decrease in herbaceous cover in a temperate forest is attributed to light deficit caused by a denser canopy. This can be a consequence of less intensive forest management or even abandonment, as well as the lack of natural disturbance including the activities of grazers (
The majority of the temperate forest resurvey studies document high species turnover, as a consequence of environmental change. Denser canopies effect not only the cover of the herbaceous layer, but also trigger trait-based reactions as the decrease in light-demanding species and increase in species with good abilities for living in shade (
Our results support the concept that the experienced intensive fine-scale dynamics is profoundly governed by the stand dynamic events of the studied forest stand. Significant differences were found between the individual SDSs and between years in herbaceous cover, species richness and species turnover at the SDS-scale. Highest species richness, mean species number/plot and highest herb cover characterized the two main gaps (OCO and OBG) in 1996. An expressed decrease in the herbaceous layer cover was observed after 17 years in these two, gradually closing gaps, where the saplings have overgrown and started to cast shadow on the herbaceous plants. Lateral canopy expansion of bordering trees has also contributed to gap closure. A very high number of extinctions with high absolute species turnover were detected in these situations. In the old collapse (OCO) the cover of Dryopteris filix-mas, Athyrium filix-femina, and Urtica dioica was drastically reduced. In the old beech gap (OBG) pronounced recession of Galium odoratum, Dryopteris filix-mas, Fagus sylvatica (young beech individuals have grown out of the herbaceous layer) and Mercurialis perennis was detected. Competition between the herbaceous plants and the saplings, especially with the very competitive beech saplings, and the resulting drop in herbaceous plant cover, was observed by several authors (Davis et al. 1998,
The Slovakian fir-beech forest investigated by
Although the four subsamples of each plot were relocated only with a 1 m accuracy in 2013, statistical tests proved that the time effect (change in vegetation) was significantly higher than the relocation effect. With this we managed to assure that the interpreted temporal changes were not artefacts resulting from imperfect relocation.
We found that intensive local-scale extinction and colonization episodes were balanced at the stand-scale, resulting in overall stability of the species pool in the herbaceous layer vegetation. These results have important implications for both forest management and conservation.
The observed stand dynamics driven changes of vegetation indicate that the use of small regeneration areas in forest management can prevent competitive ruderal species (e.g. Calamagrostis epigejos) from causing serious problems in regeneration (
From a conservation viewpoint, one of the most important species-related implications is that the long-term survival of closed forest specialists, including ancient forest indicators (
Several studies documented that habitat specialist species occur in the highest numbers in forested landscapes with long continuity of forest structures and habitats (for a review see e.g.
In areas, where nature conservation is not the sole purpose of management, managers have started to apply retention forestry as a means of integrating conservation concerns into forest management. A thorough review (
All these suggest that for successful conservation of forest biodiversity we still need to preserve existing remnants of woodlands with high conservation value and also to apply a mix of management approaches in their immediate surrounding that support natural processes and the creation of important habitats.
The authors are grateful to all those friends and colleagues who helped in any phase of the fieldwork during the original or the resurvey, especially to Péter Ódor, Erzsébet Szurdoki and Ilona Paszterkó and László Gálhidy. We thank the constructive comments and suggestion of an anonymous reviewer, which helped to improve our paper. We also thank Zoltán Botta-Dukát for his statistical advice. This work was partially supported by a grant from Switzerland through the Swiss Contribution (SH-4/13).