Patterns of forest dynamics in a secondary old-growth beech-dominated forest in the Jizera Mountains Beech Forest Reserve, Czech Republic

Abstract

Restoring the structural characteristics of secondary old-growth forests that were previously managed is increasingly debated to help increase the area of more complex forests which provide a broader array of forest services and functions. The paucity of long-term data sets in Central Europe has limited our ability to understand the ongoing ecological processes required for effective restoration programs for old-growth forests. To address this, we used repeated census data from eight permanent plots to evaluate forest structural dynamics over a 12-year period in the largest complex of European beech (Fagus sylvatica L.) forests in the Czech Highlands without intensive forestry intervention for almost 50 years. Our results showed that previously managed forests can exhibit structural qualities typically associated with old-growth forests after management has ceased for a period. The stand structural characteristics (e.g., density of large and old trees) is comparable with protected reserves of old-growth European beech-dominated forests. The average stand age was 196 years, but the oldest tree was 289 years old. The annual mortality rate was 0.43% for all species, and the U-shaped distribution indicating size-dependent mortality is likely an important process that is balanced by the turnover of new tree recruitment. During the study period, we detected that the diameter distribution tended towards a rotated sigmoid distribution. The lasting effects of the most recent forest management are evident in the scarcity of dead wood, and a prolonged process of dead wood accumulation has begun. Thus, the abandonment of all management activities in near-natural forest reserves, including dead wood removal, will ensure that the forests will develop characteristics typical of old-growth forests.

Introduction

The term “old-growth” is usually used to describe forests in a late stage of successional development that are compositionally and structurally distinct from earlier successional stages ([19]). Structural components associated with old-growth forests include multilayered canopies, large variation in tree sizes, many large and old trees, standing dead trees, and large amounts of lying dead wood ([5]). Tree diameter distribution is also a representative structural feature often used to describe old-growth forests ([36]). The reverse J-shaped form has traditionally been considered indicative of old-growth forests in a state of equilibrium ([40], [36], [8]), a condition maintained by equal mortality rates among diameter classes across the entire range of diameters ([68]). However, other studies have indicated that other forms of diameter distributions, such as a rotated sigmoid curve ([21], [38], [2]), could also be characteristic of old-growth forests. A rotated sigmoid develops from rapid growth and low mortality in trees in the mid-range diameter classes sizes, which illustrates a U-shaped mortality distribution ([38]). Effective restoration programs require a thorough understanding of forest structure. Old-growth attributes (i.e., functional and structural features associated with old-growth forests) develop naturally over time, but appropriate forest management can also facilitate their development ([5]). Active restoration entails the implementation of various management techniques, such as planting seedlings, girdling, or thinning, and passive restoration describes a situation in which no action is taken except to reduce environmental stressors, such as dead wood removals or harvesting. There is vigorous debate as to which management strategy is most suitable to implement the development of old-growth attributes. Recent studies suggest that active restoration of old-growth attributes provides alternatives to conventional even- and uneven-aged silvicultural practices ([28], [15]); however, such approaches (e.g., generating snags by girdling diseased or dying trees, cutting to a rotated sigmoid diameter distribution, and downing logs by pulling or pushing trees over) are expensive. Alternatively, passive restoration should be considered when the restoration process can be expected to achieve the desired forest structure within a feasible time period ([35]).

In Central Europe, mountain areas constitute some of the largest remnants of primary forests that have survived well into modern times ([24], [64]). Because of their inaccessibility, most were not managed until the nineteenth century. Improvements in transportation and increasing wood fuel demands for industry increased the accessibility and value of untouched forests. However, even in remote mountainous areas, the possibility of centuries of selective logging, grazing, or charcoal burning can be recognized ([50]). Large aristocratic and monastic hunting estates of the past have contributed to the protection of many untouched forests. Nowadays, forest reserves under varying protection regimes account for only 12% of the European forest area ([48]). Although the protected area network has increased substantially in the last few decades, many allow large-scale harvesting inside their boundaries and numerous areas have been illegally harvested ([31], [67]). Thus, the concepts and strategies that integrate forest habitat requirements into the management and production of other forest goods and services are mandatory for sustainable forest management and the preservation of forest biodiversity in landscape ecosystems ([5], [49]).

In the Czech Republic, conservation programs protecting forest reserves have increasingly used passive restoration methods since 2002. More than 2.000 ha of forest areas have been entirely excluded from any forest management, but that corresponds to only 0.83 % of all forests in the Czech Republic ([66]). These protected forest areas are still very small and generally consist of smaller, isolated patches, as is common in most European countries ([47]). One of those unmanaged forests is located in the Jizera Mountains Beech Forest Reserve, the largest continuous European beech (Fagus sylvatica L.) forest complex in the Czech Highlands. This area provides a unique perspective on forest changes after the implementation of passive management. However, it is uncertain how quickly forest structural complexity will change and how the transition to old-growth status will develop afterwards. As a result of climate change, accelerating rates of change in structure, composition, and mortality have been reported worldwide ([3]). Quantifying the patterns and processes in developing forests is essential for conserving biodiversity and ecosystem services. We employed repeated census plot data to quantify changes in forest structure and mortality after the cessation of active forest management, and we addressed the following questions: (i) what is the current stand structure of forests in the Jizera Mountains Beech Forest Reserve after the cessation of management? Does it already have some old-growth attributes? How do selected structural characteristics compare to those of primary old-growth forests? (ii) How much have the selected structural characteristics changed over a 12-year study period? What are the rates of mortality and new tree recruitment? What are the size-mortality trends within the nature reserve? How has diameter distribution changed during the studied period?

Methods

Study area

The study area is located in the Jizera Mountains (Jizerské hory) within the Jizera Mountains Beech Forest Reserve (Jizerskohorské bučiny), Czech Republic (Fig. 1). The reserve is situated on the northern slopes along an altitudinal gradient ranging from 360 to 1006 m a.s.l. The climate is very humid because the Jizera Mountains are the first transcontinental barrier of the humid oceanic flow from the North Sea. Annual rainfall averages range between 800 and 1700 mm and the growing season lasts from 110 to 160 days ([60]). The average annual temperatures, which are strongly related to altitude, range from 3 to 7.5 °C. The uniform bedrock consists of a significant proportion of porphyric biotite granite to granodiorite, and the northwestern portion is composed of coarse-grained porphyric biotite granite. Cambisols and podzols, the most common soils in the reserve, are strongly acidic and have high contents of poor quality humus with highly variable depth profiles ([69]).

Fig. 1 - Location of the research area in Czech Republic (Jizera Mountains Beech Forest). Reserve and core zones in the reserve. Empty squares represent the study plots (A-H).

Results

Current forest structure

An overview of structural characteristics is presented in Tab. 2. Across all study plots, F. sylvatica was the dominant tree species; it accounted for at least 85% of the basal area on all plots, and some plots contained only F. sylvatica. Among standing dead trees, F. sylvatica was also the dominant species (53% to 100% of the basal area), with the exception of one plot, where P. abies represented 53% of the basal area (Tab. 2). Tree density and basal area varied greatly among plots. The mean tree density was 204 trees ha^-1 and 20 trees ha^-1 for living and standing dead trees, respectively. On average, basal area was 35.5 m² ha^-1 and 4.9 m² ha^-1 for living and standing dead trees, respectively. Plots all had a relatively high mean DBH of living trees, with the exception of plot C, but the mean DBH of standing dead trees was slightly greater (Tab. 2). Frequency of large trees with DBH ≥ 50 cm was relatively high in all plots (Tab. 2). Density of larger living trees with DBH ≥ 80 cm varied within study plots, with an average of 17 trees ha^-1. For standing dead trees, the density varied to a lesser extent, with an average of 4 trees ha^-1. The Gini coefficient and coefficient of variation varied within study plots, but the highest values were calculated for plot C (Fig. 2). The mean volume was 558 m³ ha^-1 for living trees and 69 m³ ha^-1 for dead wood, both standing and lying dead wood. Dead wood was present in all plots, with 3 to 34% of the total volume as dead wood. Lying dead wood contributed an average of 64% of this volume, however their proportion varied among study plots and ranged from 29 to 90% (Tab. 3). All decay classes were present, however, lying dead wood in decay classes 3 and 4 represented almost 75% of the total volume of lying dead wood. The most common species among lying dead wood was F. sylvatica; the contribution of other tree species was negligible (Fig. 3).

Tab. 2 - Structural characteristics of the study plots (A-H). (1): Average value for all study plots; (2): trees with DBH ≥50 cm; (3): trees with DBH ≥80 cm; (4): mean age of five oldest trees in the plot; (5): age of the oldest tree in then plot (all oldest trees were F. sylvatica).

Variable	Status/ Stats	Year	Plots								Avg (1)
			A	B	C	D	E	F	G	H
Percentage of Fagus sylvatica (%)	Living	2015	100	92	85	100	97	100	90	91	94
	Dead		62	86	77	100	53	100	47	71	75
Mean Diameter (cm)	Living	2003	48.8	61	21.6	48.1	55.7	50	49.8	39.7	46.8
		2015	50.4	49.7	20.5	44.5	43.3	50.9	49.8	39.7	43.6
	Dead	2015	29.3	61	46.4	58.6	43.3	38.6	40.5	51.5	46.2
STD Diameter (cm)	Living	2003	14.5	17.1	21.2	27.7	17.5	25.5	28.4	18	21.2
		2015	15.7	28.9	19.2	31.7	28.7	27.6	27.1	18.3	24.7
	Dead	2015	14.3	17.9	28.7	24	15.7	5.4	22.1	25.9	19.3
Basal area (m2 ha-1)	Living	2003	29.8	33.9	31.3	36.5	29.9	40.4	40.1	29.8	34
		2015	32	35	29.9	39.9	32.8	42.9	38.2	32.9	35.5
	Dead	2015	1.8	5.9	9.3	6.5	1.1	0.8	6.5	7.1	4.9
Stem density (inds ha-1)	Living	2003	147	108	436	152	112	164	156	200	184
		2015	147	136	484	172	156	164	152	220	204
	Dead	2015	20	16	28	20	4	8	36	28	20
Large trees 50 (2) (inds ha-1)	Living	2003	83	80	52	72	80	80	68	48	70
		2015	80	76	48	80	80	84	68	56	72
	Dead	2015	7	16	24	24	8	0	16	16	14
Large trees 80 (3) (inds ha-1)	Living	2003	0	20	12	20	4	20	20	4	13
		2015	0	20	16	32	4	32	20	8	17
	Dead	2015	0	4	8	8	0	0	4	4	4
Age (years)	Mean (4)	2015	205	198	167	212	205	257	153	171	196
	Max (5)		252	237	236	220	242	289	160	173	234

Fig. 2 - Structural diversity indices. Gini coefficient (left panel) and coefficient of variation of tree diameters (right panel) indices characterizing the study plots (A-H) in 2003 (green) and 2015 (yellow). Dark green indicates a decrease of the index value during the study period.

Tab. 3 - Summary of dead wood volume on study plots (A-H) in 2015.

Variable	Status	A	B	C	D	E	F	G	H	Avg
Volume (m3 ha-1)	Living	494	520	433	716	534	726	649	391	558
	Standing dead	7	16	55	4	5	7	83	82	32
	Lying dead wood	46	36	46	38	23	16	34	51	36
	Total dead wood	53	52	101	42	28	23	117	133	69
Dead wood/ living ratio (%)		11	10	23	6	5	3	18	34	14
St. dead/ dead wood ratio (%)		13	31	54	10	18	30	71	62	36

Fig. 3 - Volume of lying dead wood (m3 ha-1) by decay classes, including recent dead (1) to the highly decayed wood (5), and species on study plots (A-H) in 2015. (FASY): Fagus sylvatica; (PIAB): Picea abies; (ABAL): Abies alba; (ACPS): Acer pseudoplatanus; (SOAU): Sorbus aucuparia.

The oldest tree was a 289-year old F. sylvatica (on plot F). The maximum age of A. pseudoplatanus and P. abies was estimated to be 165 and 153 years old, respectively. The average of the mean plot ages was 196 years, with a range of 153 to 257 years (Tab. 2). Tree establishment occurred irregularly throughout the last three centuries. There were four peaks observed around 1770, 1800-1810, 1850-1870, and 1960 (see Fig. S1 in Supplementary material), and relatively long periods of four decades or more with little tree establishment. The evaluation of the relationship between tree age and diameter among F. sylvatica was best described by a third polynomial regression (n = 77, R² = 0.698 - Fig. 4).

Fig. 4 - Relationship between tree age and tree diameter from all study sites. Loess curve with the 95% confidence interval is reported for the relationship of Fagus sylvatica species. (FASY): Fagus sylvatica; (PIAB): Picea abies; (ACPS): Acer pseudoplatanus; (ACPL): Acer platanoides; (SOAU): Sorbus aucuparia.

Changes in forest structural characteristics

The most variable stand characteristic over time was the density of large trees ≥ 80 cm DBH with a mean increase of 32.0% (Tab. 2). Other structural attributes were much less variable over time; value increases were +10.6% for stem density, +4.4% for basal area, and +1.6% for density of large trees > 50 cm DBH. Standard deviation of diameter displayed a relatively sustained increase of 16.1%. No major changes in species composition were observed between the two measurements. Changes in the structural diversity indices varied greatly among study plots, whereas the overall mean increase was 13.1% for the coefficient of variation and 19.4% for the Gini coefficient (Fig. 2). The highest change of structural indices was observed on plot E. The size-mortality trend was asymmetrically U-shaped for all study sites. Annual mortality rates declined from about 0.3% in the smallest diameter class to 0.1% in the 20-cm class, and then it increased to about 0.8% in classes ≥ 70 cm DBH (Fig. 5). During the 12-year study period, the overall mortality rate was 0.43% year^-1 (19 dead of 376 living trees in 2003 - see Tab. S1 in Supplementary material). Three trees were uprooted, and two trees had a broken stem, but they were still alive. The highest mortality rate was observed on plot B (0.64% year^-1), and the lowest was on plot A (0.19% year^-1). Mortality rates were balanced by the turnover of new tree generations. The generally high recruitment rates during the study period varied among plots; the highest observed densities were on plots C and E. The most abundant species in the recruitment layer (5 to 20 cm DBH) was F. sylvatica; P. abies, A. platanoides, and S. aucuparia were also present in low densities.

Fig. 5 - Observed annual mortality rate by size class (5-9.9 cm, 10-29.9 cm, 30-49.9 cm, 50-69.9 cm, and ≥ 70 cm) at the study plots (A-H). Numbers in white above each bar indicate the sample size (number of living trees in 2003).

Live tree diameter distribution of the study forest was dominated by F. sylvatica across all diameter classes. Most plots consisted of F. sylvatica in the upper canopy with P. abies in the mid-canopy, and other species were most common in the lower canopy. The change in the forest level diameter distribution between 2003 and 2015 reflected a convergence to a rotated sigmoid shape (Fig. 6). The plot level diameter distribution displayed a variety of structures in 2003, often with a tendency towards unimodal distributions, although the reverse J-shaped form was the best fit for study plot C. Over time, the rotated sigmoid curves were evident in most plots (B, C, D, E, F) in 2015. The other plots (A, G, H) remained stable over time and they had unimodal shapes (see Fig. S2 in Supplementary material). Moreover, the changes were not significant for any of the plots over time (Tab. S2). Size structure was adequately predicted by the third-degree polynomial function, and it proved to be a better fit than the Kernel function.

Fig. 6 - Forest level diameter distribution. Cumulative empirical diameter distributions in 2003 (left) and 2015 (right). The solid lines represent the third-degree polynomial function (red) and the Kernel function (blue) for all living trees. Individual trees are grouped into 5 cm diameter classes. (FASY): Fagus sylvatica; (PIAB): Picea abies; (ACPS): Acer pseudoplatanus; (ACPL): Acer platanoides; (SOAU): Sorbus aucuparia.

Discussion

Current forest structure

The core zones of the Jizera Mountains Beech Forest Reserve are composed of relatively structurally heterogenous forests. They contain many large and old trees, multilayered canopies, and high variation in tree size and age, all structural characteristics typically associated with old-growth forests ([5]). The structural attributes were comparable with other abandoned European beech-dominated forest reserves or primary old-growth forests in Europe (Tab. 4). With the exception of lower dead wood volumes, which are undergoing an accumulation process, the other structural parameters were within the ranges reported by other studies.

Tab. 4 - Structural data for old-growth European beech-dominated forests. (1): This study (Jizera Mountains Beech Forest); (2): [32] (Zofín); (3): [24] (Hrončecký grún); (4): [34] (Stužica); (5): [46] (Labowiec); (6): [10] (Uholka); (7): [29] (Janj); (8): [42] (Lom); (9): [10] (Sihlwald); (10): [43] (Ludrin); (11): [6] (mean for old-growth European beech-dominated forests); (12): for the study period 2001-2010; (13): standing and lying dead wood. Bedrock: (gr) granite; (an) andesite; (fl) flysch; (li) limestone. Soils: (ca) cambisols; (po) podzols; (re) rendzina. (∞): Considered as a primary forest; (Qmd): Quadratic mean diameter.

Variable	Status	Country
		CZ1	CZ2	SK3	SK4	PL5	UA6	BA7	BA8	CH9	IT10	EU11
Last management	-	1960	1882	∞	∞	1957	∞	∞	1956	1995	1962	-
Altitude (m a.s.l.)	-	671	780	890	1075	900	750	1330	1386	650	1300	-
Bedrock	-	gr	gr	an	fl	fl	fl, li	li	li	-	li	-
Soils	-	ca, po	ca, po	ca	ca	ca	-	ca, re	re	ca	ca	-
Age (years)	-	196	169	-	-	-	150	-	-	150	-	-
Basal area (m2 ha-1)	Living	35.5	40.9	41.8	38.2 12	36.3	38.5	66.7	47.1	30.7	45.1	39.9
Qmd (cm)	Living	47.1	50.3	46.8	38.1	-	47.3	40.6	35.0	38.9	27.8	64.9
Density (trees ha-1)	Living	204	206	243	336	-	219	516	489	259	741	447
	Living 50	72	-	-	-	73	-	115	99	-	52	94
	Living 80	17	-	6	12	-	21	42	18	-	0	-
Volume (m3 ha-1)	Living	558	695	724	560	543	770	1215	763	524	533	-
	Standing dead	32	-	25	-	-	-	80	91	-	8	-
	Lying dead	36	202 13	281	133	383 13	111	307	236	8 13	70	193 13
Dead/ living ratio (%)		14.0	22.3	-	23.7	-	13.0	-	42.9	1.4	-	-

The importance of disturbances in dead wood dynamics is well documented ([9], [41], [39]). Each disturbance type has characteristic frequency and intensity patterns, which produces important differences in the spatial and temporal distribution of dead wood. Natural disturbance regimes in European temperate deciduous forests are characterized by mixed disturbance severity regimes, a combination of frequent, small-scale events, and occasional moderate to high-severity events, predominantly caused by storms and drought ([16], [62], [44]). Mixed disturbance severity regimes tend to generate irregular inputs of dead wood, with a wide range of sizes, shapes, and decay classes present ([9]). Christensen et al. ([9]) reported an average of 132 m³ ha^-1 of dead wood for primary and long-established European beech-dominated forest reserves. Burrascano et al. ([6]) observed higher dead wood quantities (mean = 193 m³ ha^-1) in a European dataset of old-growth forests. Other studies of European beech-dominated forests indicate a natural range of 78 to 387 m³ ha^-1 (Tab. 4). In Poland, Paluch ([46]) observed more than 380 m³ ha^-1 of dead wood in the Labowiec Forest Reserve, which was similar to findings from the Janj Forest Reserve in Bosnia and Herzegovina ([29]). In our study, forests with no management for more than 50 years had from 23 to 133 m³ ha^-1 of dead wood, which is much lower than reported in other studies. Based on the dead to live wood ratio, the observed average value of 14% was lower than the mean ratio of 21% for recently-established mountain forest reserves ([9]). According to a review by Burrascano et al. ([6]), our plots fall in the lower part of the range (6-89%). This pattern is likely related to the more recent soft silvicultural practices (targeted tree gridling, dead wood removal, or understory thinning). On average, standing dead trees represented 36% of the dead wood recorded, but the proportion varied among plots (from 10 to 71%). This was consistent with the percentage of standing dead wood in other old-growth beech-dominated forests, which ranged from 16 to 47% ([9], [63]). The high volume of standing dead trees on plot G was likely due to the higher abundance of coniferous trees, which are generally larger and their decay slower than most deciduous trees ([50]). All dead wood decay classes were found among the study sites, but the most advanced class (5) was relatively infrequent. This is likely associated with the past silvicultural practices, which likely reduced overall mortality and dead wood inputs ([37]). Some studies have suggested that in the absence of major disturbances, dead wood accumulation in managed forests with no management is a slow process ([63], [41]). Peterken ([50]) suggested that accumulation of near natural volumes of dead wood could occur within a century. Comparing our results to dead wood stocks from primary old-growth forests or reserves abandoned for more than 100 years suggests that our studied forest reserve is at the beginning of a long process of dead wood accumulation ([33], [9], [41]). The retention of dead wood as well as artificial creation of dead wood have been identified as the key approaches to successful dead wood management in forests where the aim is to maintain biodiversity ([65]).

Living tree density and basal area were also comparable with other studies of old-growth European beech-dominated forests. According to a review by Burrascano et al. ([6]), the mean values of basal area and stem density were higher than the values reported in our study. Our plots had a higher quadratic mean diameter (47.1 cm) compared to other studies from Europe ([10], [24], [34], [42], [29], [43]); however, Burrascano et al. ([6]) reported slightly higher values (mean of 64.9 cm) within old-growth European beech-dominated forests. The presence of large trees is considered one of the most important features of old-growth forests. Large F. sylvatica trees play a unique and critical role in supporting diversity of other organisms, such as birds ([13]) and lichens ([23]). Burrascano et al. ([6]) reported a minimum threshold of large tree density for old-growth forests at a global scale (30 trees with DBH ≥ 50 cm), which was observed in our study, but the mean value for European beech-dominated forests is considerably higher. Frequency of larger trees with DBH ≥ 80 cm was similar to the values found in other old-growth European beech-dominated forests.

Tree age analysis revealed that the age distribution was multimodal (Fig. S1 in Supplementary material), a pattern commonly found in old-growth beech-dominated forests in Central Europe ([33], [62]). Four recruitment peaks were evident around 1770, 1800-1810, 1850-70, and 1960. The number of old trees in our sample was relatively low, so some of the oldest recruitment periods, such as 1770 to 1810, were difficult to interpret. The longer frequent recruitment period from 1850 to 1870 has also been observed in other Bohemian (Zofín) and Carpathian (Uholka) beech-dominated forest reserves; a higher frequency of strong windstorms has been identified during this period for the region ([62], [55]). The obvious rise in tree recruitment after 1960 can be linked to the mortality of older trees; as older cohorts begin dying, recruitment of a new generation of trees begins. Cautiously, we cannot exclude limited historical human impact in this area that may have influenced recruitment rates. The age distribution also helped explain the sigmoid form of the diameter distribution (Fig. 6); it displayed a more or less pronounced peak in the midsize diameters ([62]). At least one F. sylvatica more than 250 years old was found, but that is younger than the oldest tree (409 years old) previously reported for the Czech Republic ([7]). According to Di Filippo et al. ([14]), the maximum and mean age of the three to five oldest trees are good indicators to evaluate old-growth status. Thus, the observed plot mean age of the oldest trees (196 years) demonstrated a characteristic feature of studied old-growth forests, a period when the mean canopy age is at least half the maximum lifespan of the dominant tree species ([62]). The old-growth status of a stand can also be characterized by high variability in tree ages within a given diameter class (Fig. 4), which reflects the complex dynamics of uneven-aged forests ([52], [62], [14]).

Changes in forest structural characteristics

Our study highlighted the changes of old-growth features over time since the last forest management interventions; most notably, the density of very large trees, structural diversity, and diameter structure. The U-shaped mortality pattern is characteristic of old-growth forests. Indeed, the relatively high numbers of recruited trees demonstrate the dynamics of the natural regeneration process.

The greater change over time was observed in the density of large living trees with DBH ≥ 80 cm; changes in the density of smaller trees (DBH ≥ 50 cm) did not increase as much. Variability in living stem density between measurements was twice as high as that of basal area, as indicated by the relatively high change in stem numbers observed in the lower tree layers (5 to 20 cm DBH). The increased basal area could also be interpreted as another indicator of the changes towards more natural forest structures, as harvesting activities in managed forests typically prevent stand basal area from reaching such high values ([22]). Also, average temporal changes of structural indices showed slight increases (Fig. 2). The DBH differentiation, expressed as the Gini coefficient, was similar to values observed in unmanaged forests of the Carpathians ([45]). Our results reflect the general pattern that even-aged forests are more homogenous than uneven-aged forests, as suggested by Sterba & Zingg ([58]). The highest Gini indices were found within mixed uneven-aged plots, and pure even-aged plots, which were relatively homogenous, had the lowest Gini indices. Large tree size diversity may ensure a wide range of habitats and provide higher levels of biodiversity in forest ecosystems ([45], [30]).

The diameter structure of the study forest changed over time to a typical rotated sigmoid pattern. Changes in tree numbers were most evident in the smallest diameter classes compared to 2003. The higher number of trees frequently found in the midsize diameters range elucidates a common trend towards a rotated sigmoid diameter distribution. The diameter structures of individual plots indicated variability at the beginning of the study period. Most plots converged towards a rotated sigmoid diameter distribution over time, even the plot with reverse J-shaped diameter structure. In a few plots the diameter structure did not change substantially and they reflected a unimodal structure at the end of the study period. The rotated sigmoid curve of diameter distribution is commonly observed in old-growth forests dominated by F. sylvatica ([68], [2], [62]). Various studies from North America have also reported diameter distributions of a rotated sigmoid form for various mixed-species forests ([21], [38]). Westphal et al. ([68]) indicated three main mechanisms, including infrequent disturbance events, mortality, and nonlinear diameter growth rates, which likely explain the rotated sigmoid structure. A mixed disturbance severity regime and associated regeneration can create discontinuous and unbalanced diameter structures. Non-constant mortality rates with a lower mortality rate for all trees that successfully reached the upper canopy level and increased mortality rates for very large trees results in mid-size peaks in diameter distributions. The third factor that drives the development of a rotated sigmoid curve is a positive relationship between diameter increment and stem size ([68]). The empirical diameter distributions were most precisely predicted by a third-degree polynomial function, which is commonly used to model diameter distributions ([68]).

The U-shaped mortality trend with minimum mortality rates in the midsize classes corresponded to the current diameter structure that appeared to be converging towards a rotated sigmoid curve (Fig. 6). Complete U-shaped mortality has been reported in several old-growth beech-dominated forests throughout Europe ([2], [26]). Larger trees are more susceptible than medium-sized trees to insect attacks, drought, rot, and mechanical instability during storms ([25], [26]). The mortality of small-sized trees is mostly attributed to competition, whereby smaller trees have to compete against larger trees for light, water, and nutrients ([1], [11]). Annual mortality rates for all species were 0.43% on average, but that is lower than rates (more than 1%) reported for other old-growth beech-dominated forests in Central Europe ([25], [26]). Tree mortality rates are typically low in the absence of larger disturbances ([50]). Together with observed increases in the density of large trees and basal area in our study forest, the increase in mortality is predictable given the forest age. However, the mortality rates are balanced in the turnover of new tree generations, and the stand gradually again advances to the high growth rate stage of development. Species-specific mortality has been suggested to account for contrasting life history strategies, lifespan, competitiveness, and varying responses to abiotic factors ([18], [25]).

Conclusions

Our study of the Jizera Mountains Beech Forest Reserve core area over a 12-year period found persistent transition of the forest towards natural states after more than five decades without management. The study area displayed a variety of old-growth characteristics (e.g., density of large, old trees, structural heterogeneity, diameter distribution, and mortality), which is consistent with previously reported studies on primary old-growth forests or reserves that had never been managed or unmanaged for even longer time periods. The impacts of past management are still visible in the low amounts of dead wood, but the reserve is at the beginning of a long process of dead wood accumulation. As forest development progresses, the death of old trees allows for higher recruitment into the understory and it enhances the growth rates of the surviving trees; this pulse in recruitment cycles and dead wood accumulation will continue in the absence of disturbance or management. Although our study is based on a repeated census dataset covering 12 years, this time span is still very short relative to both the longevity of trees and forest succession. The monitoring of secondary old-growth forest reserves and maintaining forest ecosystem services will help ensure responsible stewardship for integrative forest management that aims to address ecological, economic, and social issues across entire forests over time.

Acknowledgements

This study was supported by IGA project (B0917) financed by the Internal Grant Agency of FFWS CULS in Prague, institutional project “EVA4.0” (CZ.02.1.01/0.0/0.0/16_019/0000803) and project INTER-COST (LTC17055) financed by Ministry of Education, Youth and Sports of Czech Republic. We especially thank to J. Trešnák for providing all data from his diploma thesis. We would like to thank P. Uzel, M. Trčka, J. Hanousek, M. Matouš, D. Hetešová, F. Chrapan, and S. Komín for assistance in the field. We would also like to thank the Jizera Mountains Protection Landscape Area authorities, especially V. Vršovský, for administrative support. Also, thanks to the anonymous reviewers for their helpful and constructive reviews.

JL designed the methods, carried out surveys, measurement and analysis, coordinated the research team, developed and wrote the manuscript, RCM performed the language revision and helped to draft the manuscript, VT helped with data analysis, PJ, RB, VC, MM, HM and JSS helped with writing the manuscript, KS, LM, MS helped with the laboratory measurement, MS conceived the study and helped to draft the manuscript.

References

(1) Adler FR (1996). A model of self-thinning through local competition. Proceedings of the National Academy of Sciences USA 93: 9980-9984.

(2) Alessandrini A, Biondi F, Di Filippo A, Ziaco E, Piovesan G (2011). Tree size distribution at increasing spatial scales converges to the rotated sigmoid curve in two old-growth beech stands of the Italian Apennines. Forest Ecology and Management 262: 1950-1962.

(3) Allen CD, Breshears DD, McDowell NG (2015). On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6: 1-55.

(4) Assmann E (1961). Waldertragskunde. Organische production, Struktur, Zuwachs und Ertrag von Waldbestanden [The principles of forest yield study: studies in the organic production, structure, increment and yield of forest stands]. BLV Verlagsgesellschaft, Munchen, Bonn, Wien, pp. 490. [in German] Gscholar

(5) Bauhus J, Puettmann K, Messier C (2009). Silviculture for old-growth attributes. Forest Ecology and Management 258: 525-537.

(6) Burrascano S, Keeton W, Sabatini F, Blasi C (2013). Commonality and variability in the structural attributes of moist temperate old-growth forests: a global review. Forest Ecology and Management 291: 458-479.

(7) Cada V (2014). Dlouhovekost buku lesního [The longevity of Fagus sylvatica]. Šumava 4: 10-11. [in Czech] Gscholar

(8) Cancino J, Von Gadow K (2002). Stem number guide curves for uneven-aged forests - development and limitations. In: “Continuous Cover Forestry” (Von Gadow K, Nagel J, Saborowski J eds). Springer, Netherlands, pp. 163-174. Gscholar

(9) Christensen M, Hahn K, Mountford EP, Odor P, Standovár T, Rozenbergar D, Diaci J, Wijdeven S, Meyer P, Winter S, Vrška T (2005). Dead wood in European beech (Fagus sylvatica) forest reserves. Forest Ecology and Management 210: 267-282.

(10) Commarmot B, Bachofen H, Bundziak Y, Bürgi A, Ramp B, Shparyk Y, Sukhariuk D, Viter R, Zingg A (2005). Structures of virgin and managed beech forests in Uholka (Ukraine) and Sihlwald (Switzerland): a comparative study. Forest Snow and Landscape Research 79: 45-56. Gscholar

(11) Coomes DA, Allen RB (2007). Mortality and tree-size distributions in natural mixed-age forests. Journal of Ecology 95: 27-40.

(12) Cybis (2014). CooRecorder and CDendro programs of the CooRecorder. CDendro package, version 7.8. Web site. Online | Gscholar

(13) Czesczewik D, Zub K, Stanski T, Sahel M, Kapusta A, Walankiewicz W (2015). Effects of forest management on bird assemblages in the Bialowieza Forest, Poland. iForest - Biogeosciences and Forestry 8: 377-385.

(14) Di Filippo A, Biondi F, Piovesan G, Ziaco E (2017). Tree ring-based metrics for assessing old-growth forest naturalness. Journal of Applied Ecology 54: 737-749.

(15) Dove NC, Keeton WS (2015). Structural complexity enhancement increases fungal species richness in northern hardwood forests. Fungal Ecology 13: 181-192.

(16) Drössler L, Von Lüpke B (2005). Canopy gaps in two virgin beech forest reserves in Slovakia. Journal of Forest Science 51: 446-457.

(17) Duncan R (1989). An evaluation of errors in tree age estimates based on increment cores in Kahikatea (Dacrycarpus dacrydioides). New Zealand Sciences 16: 31-37. Gscholar

(18) Franklin JF, Shugart HH, Harmon ME (1987). Tree death as an ecological process: the causes, consequences and variability of tree mortality. BioScience 37: 550-556.

(19) Franklin JF, Spies TA (1991). Ecological definitions of old-growth douglas-fir forests. In: “Wildlife and Vegetation of Unmanaged Douglas-Fir Forests” (Ruggiero LF, Aubry KB, Carey AB, Huff MH eds). General Technical Report, USDA Forest Service, Portland, OR, USA, pp. 61-70. Gscholar

(20) Gini C (1921). Measurement of inequality of incomes. The Economic Journal 31: 124-126.

(21) Goff FG, West D (1975). Canopy-understory interaction effects on forest population structure. Forest Science 21: 98-108. Gscholar

(22) Heiri C, Wolf A, Rohrer L, Bugmann H (2009). Forty years of natural dynamics in Swiss beech forests: structure, composition, and the influence of former management. Ecological Applications 19: 1920-1934.

(23) Hofmeister J, Hošek J, Malíček J, Palice Z, Syrovátková L, Steinová J, Cernajová I (2016). Large beech (Fagus sylvatica) trees as “lifeboats” for lichen diversity in central European forests. Biodiversity and Conservation 25: 1073-1090.

(24) Holeksa J, Saniga M, Szwagrzyk J, Czerniak M, Stasynska K, Kapusta P (2009). A giant tree stand in the West Carpathians - an exception or a relic of formerly widespread mountain European forests? Forest Ecology and Management 257: 1577-1585.

(25) Holzwarth F, Kahl A, Bauhus J, Wirth C (2013). Many ways to die - partitioning tree mortality dynamics in a near-natural mixed deciduous forest. Journal of Ecology 101: 220-230.

(26) Hülsmann L, Bugmann HKM, Commarmot B, Meyer P, Zimmermann S, Brang P (2016). Does one model fit all? Patterns of beech mortality in natural forests of three European regions. Ecological Applications 26: 2463-2477.

(27) IFER (2008). Field-Map technology, version 8. IFER-Monitoring and Mapping Solution Ltd., Web site. Online | Gscholar

(28) Keeton WS (2006). Managing for late-successional/old-growth characteristics in northern hardwood-conifer forests. Forest Ecology and Management 235: 129-142.

(29) Keren S, Motta R, Govedar Z, Lucic R, Medarevic M, Diaci J (2014). Comparative structural dynamics of the Janj mixed old-growth mountain forest in Bosnia and Herzegovina: are conifers in a long-term decline? Forests 5: 1243-1266.

(30) Kozák D, Mikoláš M, Svitok M, Bače R, Paillet Y, Larrieu L, Nagel TA, Begovič K, Cada V, Diku A, Frankovič M, Janda P, Kameniar O, Keren S, Kjučukov P, Lábusová J, Langbehn T, Málek J, Mikac S, Morrisey RC, Nováková MH, Schurman JS, Svobodová K, Synek M, Teodosiu M, Toromani E, Trotsiuk V, Vítková L, Svoboda M (2018). Profile of tree-related microhabitats in European primary beech-dominated forests. Forest Ecology and Management 429: 363-374.

(31) Knorn J, Kuemmerle T, Radeloff VC, Szabo A, Mindrescu M, Keeton WS, Abrudan I, Griffiths P, Gancz V, Hostert P (2012). Forest restitution and protected area effectiveness in post-socialist Romania. Biological Conservation 146: 204-212.

(32) Král K, Janík D, Vrška T, Adam D, Hort L, Unar P, Samonil P (2010). Local variability of stand structural features in beech dominated natural forests of Central Europe: implications for sampling. Forest Ecology and Management 260: 2196-2203.

(33) Korpel S (1995). Die Urwalder der Westkarpaten [The old-growth forests of Western Carpathians]. Gustav Fischer Verlag, Stuttgart, Austria, pp. 310. [in German] Gscholar

(34) Kucbel S, Jaloviar P, Saniga M, Vencurik J, Klimaš V (2010). Canopy gaps in an old-growth fir-beech forest remnant of Western Carpathians. European Journal of Forest Research 129: 249-259.

(35) Lachat T, Bütler R (2009). Identifying conservation and restoration priorities for saproxylic and old-growth forest species: a case study in Switzerland. Environmental Management 44: 105-118.

(36) Leak WB (1964). An expression of diameter distribution for unbalanced, uneven-aged stands and forests. Forest Science 10: 39-50. Gscholar

(37) Lombardi F, Chirici G, Marchetti M, Tognetti R, Lasserre B, Corona P, Barbati A, Ferrari B, DiPaolo S, Giuliarelli D, Mason F, Iovino D, Nicolaci A, Bianchi L, Maltoni A, Travaglini D (2010). Deadwood in forest stands close to old-growthness under Mediterranean conditions in the Italian Peninsula. Italian Journal of Forest and Mountain Environments 65: 481-504.

(38) Lorimer CG, Dahir SE, Nordheim EV (2001). Tree mortality rates and longevity in mature and old-growth hemlock-hardwood forests. Journal of Ecology 89: 960-971.

(39) Meigs GF, Morrissey RC, Bače R, Chaskovskyy O, Cada V, Després T, Donato CD, Janda P, Lábusová J, Seedre M, Mikoláš M, Nagel TA, Schurman JS, Synek M, Teodosiu M, Trotsiuk V, Vítková L, Svoboda M (2017). More ways than one: mixed-severity disturbance regimes foster structural complexity via multiple developmental pathways. Forest Ecology and Management 406: 410-426.

(40) Meyer HA (1952). Structure, growth, and drain in balanced uneven-aged forests. Journal of Forestry 52: 85-92. Gscholar

(41) Meyer P, Schmidt M (2011). Accumulation of dead wood in abandoned beech (Fagus sylvatica L.) forests in northwestern Germany. Forest Ecology and Management 261: 342-352.

(42) Motta R, Berretti R, Castagneri D, Dukić V, Garbarino M, Govedar Z, Lingua E, Maunaga Z, Meloni F (2011). Toward a definition of the range of variability of central European mixed Fagus-Abies-Picea forest Lom (Bosnia and Herzegovina). Canadian Journal of Forest Research 41: 1871-1884.

(43) Motta R, Garbarino M, Berretti R, Meloni F, Nosenzo A, Vacchiano G (2015). Development of old-growth characteristics in uneven-aged forests of the Italian Alps. European Journal of Forest Research 134: 19-31.

(44) Nagel T, Svoboda M, Kobal M (2014). Disturbance, life history traits, and dynamics in an old-growth forest landscape of southeastern Europe. Ecological Applications 24: 663-679.

(45) Pach M, Podlaski R (2015). Tree diameter structural diversity in Central European forests with Abies alba and Fagus sylvatica: managed versus unmanaged forest stands. Ecological Research 30: 367-384.

(46) Paluch JG (2007). The spatial pattern of a natural European beech (Fagus sylvatica L.)-silver fir (Abies alba Mill.) forest: a patch-mosaic perspective. Forest Ecology and Management 253: 161-170.

(47) Parviainen J, Bucking W, Vandekerkhove K, Schuck A, Päivinen R (2000). Strict forest reserves in Europe: efforts to enhance biodiversity and research on forests left for free development in Europe (EU-COST-Action E4). Forestry 73: 107-118.

(48) Parviainen J, Schuck A, Bozzano M, Estreguil C, Koskela J, Lier M, Spielmann M, Van Brusselen J (2011). Criterion 4: maintenance, conservation and appropriate enhancement of biological diversity in forest ecosystems. In: “State of Europe’s Forests 2011, Status and Trends on Sustainable Forest Management in Europe”. FOREST EUROPE, UNECE and FAO, Aas, Norway, pp. 65-97. Online | Gscholar

(49) Persiani AM, Lombardi F, Lunghini D, Granito VM, Tognetti R, Maggi O, Pioli S, Marchetti M (2015). Stand structure and deadwood amount influences saproxylic fungal biodiversity in Mediterranean mountain unmanaged forests. iForest - Biogeosciences and Forestry 9: 115-124.

(50) Peterken GF (1996). Natural woodland: ecology and conservation in northern temperate regions. Cambridge University Press, Cambridge, UK, pp. 540. Gscholar

(51) Petráš R, Pajtík J (1991). Sústava česko-slovenských objemových tabuliek drevín [Forest tree volume tables of the CSFR]. Lesnický Casopis 31: 323-333. [in Czech] Gscholar

(52) Piovesan G, Di Filippo A, Alessandrini A, Biondi F, Schirone B (2005). Structure, dynamics and dendroecology of an old-growth Fagus forest in the Apennines. Journal of Vegetation Science 16: 13-28. Gscholar

(53) Rinntech (2010). TSAP-WinTM: time series analysis and presentation for dendrochronology and related applications, version 4.69h. Web site. Online | Gscholar

(54) RStudio Team (2016). RStudio: integrated development for R. RStudio, version 1.0.136, web site. Online | Gscholar

(55) Samonil P, Dolezelová P, Vašíčková I, Adam D, Valtera M, Král K, Janík D, Sebková B (2013). Individual-based approach to the detection of disturbance history through spatial scales in a natural beech-dominated forest. Journal of Vegetation Science 24: 1167-184.

(56) Sheil D, May RM (1996). Mortality and recruitment rate evaluations in heterogenous tropical forests. Journal of Ecology 84: 91-100.

(57) Sippola AL, Renvall P (1999). Wood-decomposing fungi and seed tree cutting: a 40 year prespective. Forest Ecology and Management 115: 183-201.

(58) Sterba H, Zingg A (2006). Abstandsabhängige und abstandsunabhängige Bestandesstrukturbeschreibung [Distance-dependent and distance-independent structure description]. Allg Forst-Jadztg 177: 169-176. [in German] Gscholar

(59) Stokes MA, Smiley TL (1986). An introduction to tree-ring dating. University of Chicago Press, Chicago, IL, USA, pp. 73. Gscholar

(60) Tolasz R, Miková T, Valerianová A, Voženílek V (2007). Klimatický atlas Ceska [Climate atlas of Czechia]. Ceský hydrometeorologický ústav a Palckého Univerzita v Olomouci, Praha, olomouc, Czech Republic, pp. 256. [in Czech] Gscholar

(61) Trešnák J (2004). Produkční dusledky ponechání části lesa spontánnímu vývoji v oblasti Jizerskohorských bučin [The production of forest left to spontaneous development in the Jizera beech forest]. Diplomová práce, Fakulta lesnická a environmentální, CZU v Prague, Czech Republic, pp. 51. [in Czech] Gscholar

(62) Trotsiuk V, Hobi ML, Commarmot B (2012). Age structure and disturbance dynamics of the relic virgin beech forest Uholka (Ukrainian Carpathians). Forest Ecology and Management 265: 181-190.

(63) Vandekerkhove K, De Keersmaeker L, Menke N, Meyer P, Verschelde P (2009). When nature takes over from man: dead wood accumulation in previously managed oak and beech woodlands in North-western and Central Europe. Forest Ecology and Management 258: 425-435.

(64) Veen P, Fanta J, Raev I, Biris IA, Smidt J, Maes B (2010). Virgin forests in Romania and Bulgaria: results of two national inventory projects and their implications for protection. Biodiversity and Conservation 19: 1805-1819.

(65) Vítková L, Bače R, Kjučukov P, Svoboda M (2018). Deadwood management in Central European forests: key considerations for practical implementation. Forest Ecology and Management 429: 394-405.

(66) Vrška T, Hort L (2008). Odkdy a proč chráníme samovolné procesy? [Since and do we protect the spontaneous processes?] Lesnická Práce 7: 464-466. [in Czech] Gscholar

(67) Vysoky J, Jasík M (2015). Pralesov je na Slovensku málo a ani tie nedokážeme efektívne chránit [There is a few old-growth forests in Slovakia and we cannot even protect them]. Tlačová správa, PRALES, o.z., web site. Online | Gscholar

(68) Westphal C, Tremer N, Von Oheimb G, Hansen J, Von Gadow K, Härdtle W (2006). Is the reverse J-shaped diameter distribution universally applicable in European virgin beech forests? Forest Ecology and Management 223: 75-83.

(69) Zatloukal V, Beranová J, Holá S, Litschmann P, Vopenka P, Višnák R (2010). Plán péče o Národní prírodní rezervaci Jizerskohorské bučiny na období 2012-2020 [Forest care plan management of the Jizera Mountains Beech Forest Reserve for the period 2012-2020]. Správa CHKO Jizerské hory, Liberec, Czech Republic, pp. 280. [in Czech] Gscholar