The Importance of Stand Structure in Narrow-Leaved Ash (Fraxinus angustifolia Vahl) Dieback—Insights from an Extensively Managed Stand on a Humogley Soil in Serbia ^†

Abstract

Ash dieback is a major issue affecting European ash populations, including narrow-leaved ash (Fraxinus angustifolia Vahl). An important factor contributing to the decline of narrow-leaved ash is the fungal disease caused by Hymenoscyphus fraxineus. However, the mortality of trees also depends on stand structure that may influence the disease dynamics. In 2020, we analysed the stand structure of middle-aged, extensively managed, narrow-leaved ash stands growing on Humogley soil (Cariceto remotae-Fraxinetum angustifoliae, Jov., et Tom. 1979). This permanent sample plot is located in Posavina (Serbia), where we observed reduced tree vitality and mortality. The stand originates from natural regeneration after a succession of marsh habitats. At ages 20–25 years (1996) and 30–35 years (2006), selective thinning was carried out. Until the age of 45–50 years (2020), the stand was left unthinned, and the presence of ash dieback fungus was recorded in Serbia. In 2020, we measured the diameter at breast height (DBH) of each tree on the plot and assessed their crown class and degree of isolation. These parameters were evaluated in relation to the crown defoliation of the trees. The results indicate that reduced vitality and mortality of trees manifest in conditions of strongly expressed intraspecific competition in the stand, particularly during the stem exclusion stage. Healthy trees were observed primarily within the predominant/dominant crown class and exhibited the highest mean DBH. Trees classified as dead or dying (81%–100% defoliation) had a lower mean DBH compared to both healthy trees (<25% defoliation) and significantly defoliated trees (26%–80%). This was observed at both the stand level and in predominant/dominant trees, suggesting that tree mortality is primarily linked to their poor growth.

1. Introduction

Narrow-leaved ash (Fraxinus angustifolia Vahl), ecologically an invaluable species in lowland floodplain ecosystems, is currently facing decline due to a disease caused by the ash dieback fungus Hymenoscyphus fraxineus (T. Kowalski), Baral, Queloz and Hosoya. Ash dieback has been an ongoing issue for over two decades in European ash (Fraxinus excelsior L.) [1], while in F. angustifolia, the disease was definitively reported in 2010 [2]. The disease was reported in manna ash (Fraxinus ornus L.) as well, but currently, it does not impose any major threat as this species can be considered resistant [3,4]. The disease caused by H. fraxinues is considered to be the main biotic factor in the current narrow-leaved ash decline and dieback in Posavina [5]. In Serbia, the presence of H. fraxineus on narrow-leaved ash has been confirmed by Keča et al. [6] in 2015 and Marković et al. [7] in 2016. In neighbouring countries, it was reported on European ash in 2009 and narrow-leaved ash in 2011 in Croatia [8] and on European ash in Bosnia and Herzegovina in 2009 [9], Hungary in 2007 [10], and Montenegro in 2017 [11]. Two decades have passed since the first record of it on European ash in the early 1990s in N-E Poland [12] and the first record in Serbia.

The main cause of ash decline can primarily be attributed to the fungus H. fraxineus, which can reduce the vitality of trees, making room for other, more opportunistic pathogens to colonise the root and stem tissues at later stages [13]. Recent reports acknowledge that some Diplodia species may be involved in the decline [14,15,16], as well as several other pathogenic organisms, as demonstrated in Karadžić et al. [17] or Benigno et al. [18]. Although H. fraxineus is recognised as an important driver of the decline, a number of factors may contribute to the phenomenon, as highlighted recently [18,19,20,21,22]. Besides the biotic factors involving fungi, altered site conditions may determine the course of decline at the local scale. For example, narrow-leaved ash mortality is higher on former marsh sites, according to management records from Croatia [21,22]. As pointed out by Ugarković and Pleša [20], the decline is more pronounced in stands with a large number of trees. The narrow-leaved ash decline coincides with the occurrence of the disease caused by H. fraxinues. It also coincides with the absence of adequate tending measures in the stands, as revealed by Bobinac and Andrašev [23] in a comparative study of the decline of permanent sample plots in naturally formed stands on former marsh sites in Posavina and Podunavlje areas in Serbia. The complex research conducted in the Czech Republic also showed that the mortality in F. excelsior was more pronounced in young stands with a higher number of trees. Therefore, well-developed trees seemed to be able to better compensate for the influence of H. fraxineus, causing the mortality of ash to be related to forest management practices [24].

Dominant, large F. excelsior trees appear to be less susceptible to the disease, exhibiting slower progression. However, future crop trees, even under special silvicultural treatments, have been observed to die in significant numbers due to fungal infections [25]. The mortality levels in young growth [26] and pole stands (5–25 cm) [27] are relatively high in F. excelsior and most often in trees with less than average dimensions (7.86 cm) [28] facing more collar lesions compared to older trees with higher DBHs [29]. This may be related, at least in part, to the normal self-thinning process that involves high mortality during the stem exclusion stage in young stands [30]. Reduced diameter increment may point towards reduced tree vitality [31]. The diameter increment reduction can be caused by various factors, including disease, which was confirmed in F. excelsior stands [32,33]. The influence of abiotic factors, including climatic, hydrological and structural factors [20,34], as well as the effect of competition, was confirmed in F. angustifolia stands [35].

While promising results have been achieved through induced resistance methods [36], fungicide applications [37], and natural compounds like essential oils [38], the disease remains incurable in stand conditions. Currently, forest management primarily relies on site-specific silvicultural measures, as recommended for F. excelsior [39], as a potential disease prevention strategy. Therefore, silvicultural practices in narrow-leaved and European ash stands may play an important role in the dynamics of the decline.

Silvicultural measures can be used to incentivise DBH growth and tree vigour, especially in resistant trees [40], and alter the air conditions close to the ground, making them less favourable for the fungi [24,41]. Another option is resistance breeding if there is a suitable genetic potential [42]. Other ecologically acceptable options, such as the use of biocontrol agents, are still in perspective [41]. In some cases, planting ash is no longer recommended, and replanting with other species is advised (e.g., [43,44]). However, given the difficulty of finding a replacement species that can match all the desirable traits on a range of sites, as shown for F. excelsior, this approach can only be seen as a matter of compromise [45,46] or even impose potential risks if non-native species are considered [47].

Using the data from a permanent sample plot in a middle-aged stand under an extensive management regime, this paper offers a silvicultural perspective on the ongoing narrow-leaved ash decline. The diameter structure and crown development of trees across social classes were analysed. The main aim of the study was to determine the relationship between DBH of narrow-leaved ash trees and crown class (CC), degree of crown isolation (IC), and crown defoliation (CD). A specific aim was to determine the defoliation degree of predominant/dominant trees depending on their crown isolation. Our working hypothesis was that predominant/dominant trees that primarily have a free, regularly developed crown (no crown contact with neighbouring crowns or the contact is no more than 25% of the sunlit crown) would exhibit greater resistance to decline compared to trees with crown isolation. Thus, if there are enough such trees to form the main stand, the vitality of narrow-leaved ash can be fostered by silvicultural measures aimed at controlling the competition between the trees. However, if there are insufficient numbers of these trees, and our hypothesis is not supported, the stand may be vulnerable to decline caused by H. fraxineus, confirming that the long-term sustainability of narrow-leaved ash stands on the given site is in alternative measures.

2. Materials and Methods

2.1. Study Area

The study area encompasses the western part of Flat Srem in the northeast of Serbia, which is in the Sava and Bosut rivers basin. The area is a part of a 60,000 ha pedunculate oak forest complex, which may be the largest of its kind in Europe and the world, mostly falling within the territory of Croatia [48]. The research was conducted in the Management Unit “Varadin-Županja”, compartment 44 (ΨN = 44°57′20′′ i λE = 19°17′15′′). The spatial distribution of former marsh habitats from the 1970s, where the narrow-leaved ash stands were formed, and the location of the permanent sample plot are shown in Figure 1.

Since the construction of the Sava River embankment in 1934 and the regulation works for the river Bosut in 1970, the forests in the Management Unit, “Varadin-Županja’’, were within the area protected from direct flooding and thus have changed their hydrological conditions. The study area is 81–83 metres above sea level on alluvial sediments.

According to the data from the meteorological station in Sremska Mitrovica (81 metres above sea level) for 1971–1990, the mean annual air temperature was 10.8 °C, and the mean temperature in the growing season was 16.4 °C. The mean annual precipitation was 630.4 mm, and in the growing season, it was 429.9 mm. For 1991–2020, the mean annual temperature was 11.8 °C, and in the growing season, it was 17.6 °C. The mean annual precipitation was 616.1 mm, and in the growing season, it was 411.4 mm.

The permanent sample plot was established at the end of 1996 in a natural stand of narrow-leaved ash on a former damp depression (marsh). The site was characterised as a monodominant community of narrow-leaved ash with remote sedge (Carici remotae-Fraxinetum angustifoliae Jovanović et Tomić 1979) on a Humogley soil [51,52]. The site is mostly under the influence of groundwater, with waterlogging occurring at high water levels. Flood water affects the site through controlled melioration canals from the Bosut River (Figure 1).

The permanent sample plot has been maintained and thinned since before the arrival of ash dieback fungus and the subsequent decline of narrow-leaved ash in monodominant forests in this area [53]. Based on tree ring counting from a sample of stumps from the plot, the age of the stand was determined to be 20–25 years in 1996. There was no tending or thinning before plot establishment, but two thinnings were carried out experimentally afterwards. The thinnings were aimed at helping the narrow-leaved ash trees that exhibited good quality and vitality (following the procedure described by Schädelin [54]). The first thinning was carried out at the end of 1996, and the second one in 2006 at the stand age of 30–35 years [23]. Since 2006, the devitalisation of narrow-leaved ash has been noted (Supplementary Figure S1), whereas the presence of ash dieback fungus was confirmed in 2015 [6,7].

The stands of narrow-leaved ash in hygrophilous forests in Flat Srem were mostly left unthinned. Mass dieback of narrow-leaved ash occurred due to the consistent devitalisation in poorly formed stands and the occurrence of the new disease caused by the fungus H. fraxineus (Supplementary Figure S2). Affected narrow-leaved ash trees have exhibited symptoms indicative of ash dieback caused by the fungal pathogen H. fraxineus [2,3,6,11,12]. These symptoms include increased crown transparency, dieback of shoots and branches, necrotic lesions on the bark, and the characteristic “flag” symptoms of dead petioles and leaves. Also, on the fallen petioles, numerous fruiting bodies were recorded, and subsequent identification tests from the collected material in the laboratory confirmed the presence of H. fraxineus.

2.2. Measurements and Data Analysis

Diameters at breast height (DBH) and heights were measured for all trees at the end of 2020. We measured two cross diameters with an accuracy of 1 mm. For the construction of the diameter–height curve, height measurements were carried out using Vertex III (Haglöf, Långsele, Sweden) hypsometers on a subsample of trees evenly distributed across all diameter classes.

Crown classes, the degree of isolation of the crown and crown defoliation of narrow-leaved ash were determined in 2020 at a stand age of 45–50 years. Crown classes (i.e., “social height stage”) and the degree of isolation of the crown were determined according to Assmann’s classification [55], which was modified and simplified:

• Crown class 1 (CC1) was assigned to predominant/dominant trees (tree classes 1 and 2, per Kraft [56]), Crown class 2 (CC2) to co-dominant trees (tree class 3, per Kraft [56]), and Crown class 3 (CC3) to dominated and suppressed trees (tree classes 4 and 5, per Kraft [56]);
• Degree of isolation of crown 1 (IC1) was assigned to trees with a free crown, without contact with the crowns of neighbouring trees or contact up to 25% of the sunlit crown projection area. IC2 was assigned to trees with reduced crowns due to contact with neighbouring trees on one side with a contact of 25%–50% of the sunlit crown projection area. IC3 was assigned to trees with a reduced crown from two or more sides due to contact of >50% with the neighbouring trees’ sunlit crown projection area.

For dead, standing trees, the CC and IC were determined hypothetically based on available data from previous inventories and through comparisons with living trees of similar dimensions and crown class.

Crown defoliation, defined as the percentage of leaf loss, was assessed for all the trees through comparisons with the reference tree following the methodology used within the ICP Forests programme [57]. The methodology was modified for this research as the crown defoliation 5% classes were aggregated, forming seven codes for field determination. These were further aggregated into three defoliation groups (DG1–DG3) as per

Table 1. Crown defoliation of narrow-leaved ash (Fraxinus angustifolia Vahl) as per the modified ICP Forests programme classification [57].

Field Codes	0	1	2a	2b	3a	3b	4
% leaf loss	0–10	11–25	26–40	41–60	61–80	81–99	100
Defoliation groups	DG1—healthy trees		DG2—significantly defoliated trees			DG3—dying and dead trees

. The assessment took place in the middle of the growing season of 2020.

The height curve was constructed using Michaillof’s function [58]:

$$h={ae}^{-{\displaystyle \frac{b}{d}}}+1.30$$

(1)

To determine the tree volume (V), we used volume tables for narrow-leaved ash [59] with the following analytical form:

$$V=0.552246·{(0.01·d_{1.3})}^{1.9493268}·h^{0.8714008}$$

(2)

The volume of other tree species and dead narrow-leaved ash trees was determined approximately based on the measured DBH and from the height curve for narrow-leaved ash. Lorey’s mean height was determined as per the following function:

$$h_L={\displaystyle \frac{(g_1·h_1+g_2·h_2+\cdots +g_i·h_i)}{G}}$$

g_{1, 2, … i}—the basal area of trees in diameter classes;

h_{1, 2, … i}—the mean height of trees in diameter classes determined from the height curve;

G—basal area of the stand.

2.3. Statistical Analysis

The following numerical parameters were used for the determination of the diameter structure: arithmetic mean (d_a), standard deviation (S_d), coefficient of variation (CV), range (R), minimum (d_min), and maximum (d_max). The parameters of descriptive statistics were calculated using the formulas given by Field et al. [60]. The diameter structure was visualised using the “Kernel density” method [61,62,63] with an interval width of 1 cm.

Mean DBH values were compared among different CCs, ICs, and DGs at stand level (all trees collective). Specifically, within CC1 trees (predominant/dominant trees), the mean DBHs were compared among different ICs and DGs. Additionally, DBH comparisons were conducted between trees grouped using two criteria: CC and DG (for example, predominant/dominant healthy trees vs. predominant/dominant significantly defoliated trees and so forth) and CC and IC. Comparisons of tree-level breast height diameter were conducted using a one-way ANOVA [64,65]. Data processing was performed in the R environment [66]. We used the function ‘Anova’ from the car package to express significant differences [67]. The separation of mean values was accomplished with the Least Significance Difference (LSD) test using the “agricolae” package [68]. All values of p < 0.05 were considered significant. The assumptions of the one-way ANOVA were checked analytically and graphically by controlling for homoscedasticity using Levene’s test and normality of the residuals using the Shapiro–Wilk test (Supplementary Tables S1 and S2). When these conditions were not met, different data transformations were used (Supplementary Tables S3 and S4, Supplementary Figures S3 and S4). For data visualisation, the ggplot2 [69] and the gridExtra packages were used [70].

3. Results

3.1. Basic Stand Structure in 2020

At the end of 2020, there were a total of 2115 trees per hectare, with 2000 narrow-leaved ash trees. Their mean quadratic diameter was 14.0 cm, and their mean Lorey’s height was 17.0 m. In 2020, the narrow-leaved ash share in terms of number of trees, basal area, and volume was around 95%. Other species like Ulmus carpinifolia Gled., Quercus robur L., and Pyrus communis L. were individually present (

Table 2. Basic stand structure characteristics.

	N (ha−1)	G (m2∙ha−1)	V (m3∙ha−1)	dg (cm)	hL (m)	hL/dg
Total	2115	32.37	292.1	14.0	16.9	1.08
Fraxinus angustifolia	2000	30.93	280.0	14.0	17.0	1.08
Ulmus carpinifolia	58	0.44	2.9	9.8
Quercus robur	38	0.75	7.1	15.8
Pyrus communis	19	0.25	2.1	13.0

).

3.2. Growth Characteristics and Structure of Narrow-Leaved Ash Shown per Crown Class (CC)

In 2020, the mean DBH of narrow-leaved ash was in the range of 5.8–26.8 cm with variability of almost 40%. The distribution of DBHs displayed a right asymmetry and platykurtic distribution (

Table 3. Growth characteristics and diameter structure of narrow-leaved ash (Fraxinus angustifolia Vahl) shown per crown class (CC1—predominant/dominant; CC2—co-dominant; CC3—dominated and suppressed trees).

Collective	Basic Growth Characteristics at Stand Level					Descriptive Statistics of DBH
	N (ha−1)	G (m2∙ha−1)	V (m3∙ha−1)	dg (cm)	hL (m)	n	$\overline{\mathit{x}}$ (cm)	Min (cm)	Max (cm)	Sd (cm)	CV (%)	Skew	Kurt
Fraxinus angustifolia	2000	30.93	280	14.0	17.0	208	13.1	5.8	26.8	5.06	38.6	0.54	−0.55
CC1	692	19.82	200	19.1	19.3	72	18.8	12.8	26.8	3.15	16.8	0.32	−0.35
CC2	154	2.39	20.5	14.1	15.8	16	14.0	12.3	17.2	1.53	11.0	0.93	−0.07
CC3	1154	8.72	59.5	9.8	12.0	120	9.5	5.8	15.2	2.32	24.3	−0.03	−1.03

).

CC1 trees made up 34.6% of N, 64.1% of G, and 71.4% of V. Trees from CC3 made up 57.7% of N, 28.2% of G, and 21.3% of V. The share of CC2 trees was around 8% per all three growth characteristics (Table 3). The mean DBHs of trees from different crown classes ranged from 9.5 to 18.8 cm, and the differences were statistically significant between all three crown classes, as indicated by an ANOVA. Mean DBH was the highest in the CC1 collective (Figure 2). Trees from CC3 exhibited the highest variability (24.3%). The DBH distribution of CC1 trees displayed right asymmetry and a moderate platykurtic shape, while CC3 trees displayed a symmetrical and well-expressed platykurtic shape (Table 3, Figure 2).

3.3. Growth Characteristics and Structure of All Trees and Predominant/Dominant (CC1) Narrow-Leaved Ash Trees Shown per Degree of the Crown Isolation (IC)

Due to the high percentage of CC2 and CC3 trees, there was a large number of trees with poorly developed crowns in the stand. Within the whole stand, the share of narrow-leaved ash trees with IC2 and IC3 degrees was 95.7% (per N), 88.9% (per G), and 86.7% (per V). Within the CC1 collective, the share of IC2 and IC3 was similar, reaching 87.5% (per N), 82.7% (per G), and 81.4% (per V). The share of trees with IC1 was 4.3% per N, 11.1% per G, and 13.3% per V in the stand. Within CC1 trees, IC1 share was 12.5% per N, 17.3% per G, and 18.6% per V. The mean DBH of all trees from different ICs in the stand ranged from 11.6 to 22.4 cm, where IC3 had significantly lower DBHs compared to both IC1 and IC2 trees. The mean DBH of CC1 trees shown per different IC was in the range of 17.0–22.4 cm, and IC3 was characterised by significantly lower mean DBH compared to IC1 and IC2 trees (Figure 3). The lowest DBH and highest variability were observed in IC3 trees at stand level and within CC1 trees. In all trees, the diameter distribution of IC1 displayed right asymmetry and a leptokurtic shape, while IC2 and IC3 displayed weak to moderately expressed right asymmetry and a weak platykurtic shape (

Table 4. Growth characteristics and diameter structure of narrow-leaved ash (Fraxinus angustifolia Vahl) shown per the degree of crown isolation (IC1—free crown or up to 25% contact with neighbouring crowns; IC2—reduced crown from one side, contact 25%–50% with neighbouring crowns; IC3—reduced crown from two or more sides due to contact of >50% with the neighbouring crowns).

Collective	Basic Growth Characteristics at Stand Level					Descriptive Statistics of DBH
	N (ha−1)	G (m2∙ha−1)	V (m3∙ha−1)	dg (cm)	hL (m)	n	$\overline{\mathit{x}}$ (cm)	Min (cm)	Max (cm)	Sd (cm)	CV (%)	Skew	Kurt
1 IC1	87	3.43	37.2	22.5	21.2	9	22.4	19.5	26.8	2.27	10.2	0.91	0.39
1 IC2	240	7.95	80.8	20.5	19.6	25	20.4	15.7	26.2	2.47	12.1	0.27	−0.20
IC3 (all trees)	1673	19.54	162.0	12.2	15.2	174	11.6	5.8	24.2	3.87	33.5	0.55	−0.10
IC3 (CC1 trees)	365	8.43	81.9	17.1	18.4	38	17.0	12.8	24.2	3.87	14.2	0.77	1.30

¹ IC1 and IC2 trees were found only within the predominant/dominant collective (CC1).

, Figure 4).

3.4. Growth Characteristics and Diameter Structure of All Trees and CC1 Trees Divided by the Degree of Defoliation (DG)

There was a total of 33.2% of DG3 trees (defoliation > 80%) in the stand structure. Dead and dying trees comprised 23.6% and 9.6%, respectively. The share of DG3 trees in G and V was around 12%–15%. The share of healthy trees (defoliation less than 25%) was 14.9% per N, while their share in both G and V was around 30%. The share of DG2 trees (defoliation 26%–80%) was around 51% per N, G, and V. The mean diameter was in the range of 9.3–20.6 cm within DGs. All three groups were significantly different from each other. The highest mean DBH at stand level was noted in DG1 trees and lowest in DG3 trees. The diameter distribution of all DGs was characterised by moderate to strong right asymmetry. Only the DG1 displayed a shape close to normal distribution. In DG2 and DG3, a more leptokurtic shape of distribution was displayed (

Table 5. Growth characteristics and diameter structure of all narrow-leaved ash (Fraxinus angustifolia Vahl) trees divided by defoliation groups (DG1—healthy trees, defoliation < 25%; DG2—significantly defoliated trees, defoliation 26%–80%; DG3—dead and dying trees, defoliation > 80%).

Collective	Basic Growth Characteristics at Stand Level					Descriptive Statistics of DBH
	N (ha−1)	G (m2∙ha−1)	V (m3∙ha−1)	dg (cm)	hL (m)	n	$\overline{\mathit{x}}$ (cm)	Min (cm)	Max (cm)	Sd (cm)	CV (%)	Skew	Kurt
DG1	298	10.04	104.5	20.7	20.1	31	20.6	17.2	26.8	2.33	11.3	0.58	0.08
DG2	1038	15.97	141.2	14.0	16.5	108	13.4	5.8	26.2	4.06	30.3	0.69	0.58
DG3	663	4.92	34.3	9.7	12.3	69	9.3	5.8	17.8	2.97	32.1	1.01	0.58

, Figure 5).

In the total number of CC1 narrow-leaved ash trees, there was a total of 6.9% DG3 trees. Dead trees comprised 4.2% and dying trees 2.7%. Their share in total G and V was around 5%. Healthy trees (DG1) comprised 41.7% per N and around 50% per G and V. The highest share of CC1 trees was in the significantly defoliated group (DG2, 51.4%), with a share per G and V of around 45%. The mean DBH of CC1 trees was in the range of 16.2–20.7 cm, depending on the defoliation group. Trees from the DG1 collective had statistically higher DBHs compared to DG2 and DG3 within the predominant/dominant collective. A higher mean DBH within the CC1 trees was noted in healthy trees (DG1), while the lowest DBH was in the DG3 collective. The diameter distribution of CC1 trees differed among DG collectives; in DG1, the distribution displayed a right asymmetry and weak leptokurtic shape. In DG3, the distribution displayed a left asymmetry with a well-expressed platykurtic shape (

Table 6. Growth characteristics and diameter structure of narrow-leaved ash (Fraxinus angustifolia Vahl) predominant/dominant (CC1) trees shown per defoliation group (DG1—healthy trees, defoliation < 25%; DG2—significantly defoliated trees, defoliation 26%–80%; DG3—dead and dying trees, defoliation > 80%).

Collective	Basic Growth Characteristics at Stand Level					Descriptive Statistics of DBH
	N (ha−1)	G (m2∙ha−1)	V (m3∙ha−1)	dg (cm)	hL (m)	n	$\overline{\mathit{x}}$	Min (cm)	Max (cm)	Sd (cm)	CV (%)	Skew	Kurt
DG1	288	9.82	102.3	20.8	20.1	30	20.7	17.2	26.8	2.28	11.0	0.61	0.16
DG2	356	9.01	88.5	18.0	18.7	37	17.7	12.8	26.2	3.15	17.8	0.88	0.53
DG3	48	0.99	9.2	16.2	17.3	5	16.2	14.0	17.8	1.54	9.5	−0.50	−1.37

, Figure 6).

3.5. The Relations of Stand Structure and Defoliation in All Trees and Predominant/Dominant (CC1) Narrow-Leaved Ash Trees

Based on grouping the narrow-leaved ash trees using two criteria (CC and DG), we can conclude that healthy trees (DG1) are predominantly (96.6%) predominant/dominant trees, which cannot be found within dominated and suppressed trees. Conversely, dying and dead trees were primarily (91.3%) from the CC3 collective, but they were also found in the CC1 collective (7.2%). Significantly defoliated trees were mostly represented within the CC3 collective (52.7%), with a considerable share in the CC1 collective as well (34.3%) (Figure 7).

Mean DBHs of narrow-leaved ash exhibited significant differences between CC and DG collectives. Healthy predominant/dominant trees had the highest mean DBHs and were significantly different from all other groups. The lowest mean DBHs were found in CC3 trees that were significantly defoliated and dying. Mean DBHs of significantly defoliated and dying predominant/dominant trees, as well as healthy CC2 trees, were similar and somewhere between the two aforementioned significance groups (Figure 7).

Based on grouping the predominant/dominant (CC1) narrow-leaved ash trees using two criteria, IC and DG, we can conclude that healthy trees (DG1) were predominantly (53.3%) with IC2 crowns. Healthy trees with free crowns (IC1) comprised 26.6%, and healthy trees with IC3 crowns comprised 20.1% of trees. Significantly defoliated trees were mostly represented in the IC3 collective (72.8%), compared to IC2 (24.3%), while only 2.8% were in the IC1 collective. Dying and dead predominant/dominant trees were only found in the IC3 collective (Figure 8).

The mean DBH of CC1 trees, grouped by IC and DG, was the highest in healthy trees with free crowns. The differences were significantly different compared to predominant/dominant trees with IC3 crowns, regardless of their defoliation group. Healthy and significantly defoliated predominant/dominant trees with IC2 crowns, as well as significantly defoliated predominant/dominant trees with IC1 crowns, had mean DBHs that did not differ significantly from the two aforementioned groups (Figure 8).

4. Discussion

The changes in hydrological conditions in the Posavina region have caused a succession of former marsh sites towards monodominant narrow-leaved ash stands on gleysols. A similar scenario was recorded in the Croatian part of Posavina [71] and Podunavlje in Serbia on fluvisols [72].

Regarding stand productivity, gleysol and Humogley soil in Posavina (Serbia) are suboptimal for narrow-leaved ash. In the studied stand, aged 45–50 years, the mean Lorey’s height was 17 m, approximately 10 m less than observed on optimal sites on semi-gley at the same stand age [34]. Historically, gleysols were the wettest narrow-leaved ash soils with shallow groundwater and gleying occurring between 35 and 55 cm depth [52]. However, with increased air temperature and deeper groundwater levels during the last 30 years, the growth trend of the main species has been reduced [73]. Groundwater depth fluctuations have become more pronounced, ranging from 4 to 4.5 m during the extremely dry 2012 growing season to 2 to 2.5 m during the extremely wet 2010 season [74]. Therefore, gleysols became contrasting sites for hygrophilous species like narrow-leaved ash, leading to a rapid decline.

In the narrow-leaved ash stands in Posavina in Croatia, the highest intensity of narrow-leaved ash decline was noted on marsh sites [21,22]. The sites with pedunculate oak and narrow-leaved ash in this area have become more arid since the 1980s based on research in the neighbouring Spačva basin [48], with a recorded succession of vegetation [75].

This main trend in changing site conditions in Posavina (Serbia and Croatia) indicates that narrow-leaved ash regeneration and initial stand development in Serbian Posavina occurred during a period with higher moisture availability. However, subsequent development of the stand took place under drier conditions. At the end of 1996, a 20–25-year-old stand on the sample plot in this study contained 3807 trees per hectare, of which 3596 were narrow-leaved ash trees. Their quadratic mean diameter was 7.7 cm, and the mean Lorey’s height was 9.1 m. Between 1997 and 2020, 44.4% of trees have been excluded from the stand compared to the initial number of trees in 1996 [23]. By the end of 2020, the 45–50-year-old studied stand contained 2115 trees per hectare, primarily narrow-leaved ash (2000 trees). Their mean quadratic diameter was 14.0 cm, and the mean Lorey’s height was 17.0 m. Prior to 1996, the stand was left untended and unthinned. Since then, selective thinning has been experimentally applied in 1996 and 2006 to promote the best narrow-leaved ash trees in terms of quality and vitality.

We argue that the mass decline of narrow-leaved in the studied stand on Humogley soil in Posavina (Serbia) is due to a combination of factors. This includes a lack of thinning during critical development stages, along with unfavourable abiotic and biotic conditions, particularly the emergence of the new disease H. fraxineus. This is in line with several studies on European ash [28,41,76,77,78]. Thinnings may be a valuable tool in managing ash stands, as the resistance and resilience of trees to various (a)biotic stressors can be improved in this way, making heavy thinning a preferred choice in some specific cases, such as drought [79]. While heavy thinnings may be beneficial in specific cases, such as drought, they are not always recommended. For instance, heavy thinnings were not advised for F. excelsior in declining stands in Ireland [80]. As long as the thinning regime is site-adapted [39], thinnings can be advised in F. excelsior stands to increase the vitality of remaining trees [76,81] as the unthinned stands suffer more from disease compared to thinned stands [82]. In F. excelsior, ash trees that are released early from competitors may keep a higher level of vitality (Wilhelm et al., 1999 and Wilhelm, Riegel, 2013, cited by Heinze et al. [83]). However, these trees may still exhibit root collar lesions [83]. The effects of thinning in this regard are yet to be documented by strongly supported data from permanent sample plot thinning trials on F. angustifolia. The initial influence of thinning on increment in F. angustifolia stands on optimal sites in Posavina (Serbia) was reported before the occurrence of decline and dieback caused by the presence of H. fraxineus on permanent sample plots [34,84]. Crop tree management data are missing, particularly where we lack experimental evidence for F. excelsior [39]. Modifying the stand structure in both the understorey and canopy to reduce aeration and humidity, conditions less favourable for the fungus, seems to be a practical approach, as highlighted by a recent review on F. excelsior [41]. Still, the effects of silvicultural measures, including thinnings, need to be studied in more depth when observed specifically in the context of resilience to pathogens [85]. Our results are generally in line with the previous statements. In 2020, a combined total of 33.2% of trees on the sample plot were classified as dead or dying (23.6% and 9.6%, respectively; defoliation > 80%). Within the predominant/dominant category, 6.9% of trees were in this state, including 4.2% dead and 2.7% dying, respectively. Dead and dying narrow-leaved ash trees were observed to have lower DBHs compared to healthy and significantly defoliated trees, indicating a strong correlation between mortality and poor growth. The results are consistent with the conclusions drawn for F. excelsior, where symptoms of the disease were more pronounced in trees with below-average dimensions within highly stocked stands (i.e., the trees with poor growth) [39,81].

Between 2007 and 2020, 45–50-year-old stands experienced significant competition and stem exclusion, intensified by the absence of thinning operations. A substantial proportion (65.4%) of narrow-leaved ash trees were classified as co-dominant or suppressed. The perspective of still-living trees was only in the direction of a gradual exclusion from the stand structure. Within the predominant/dominant class, narrow-leaved ash trees with the free crown constituted 12.5% of the stand, equivalent to 87 trees per hectare in absolute numbers. According to the results presented by Bobinac et al. [35] for a similarly aged narrow-leaved ash stand on a former marsh site, on a fluvisol in Podunavlje (Serbia), the highest basal area increment per tree (2.4 times higher than the average) was observed in predominant/dominant tree class between the ages of 38 and 46 years. Predominant/dominant trees with IC2 crowns exhibited a 1.4-fold increase in basal area increment compared to average, while those with IC3 crowns had only 50% of the average increment. In the studied stand, the lowest mean diameter was recorded among suppressed trees with IC3 crowns. Within predominant/dominant trees, IC3 trees displayed the lowest DBH values, indicative of impaired growth. In 2017, a mass decline of trees occurred in the stand, leading to the downward shift of crown classes for some trees, particularly those with reduced growth potential [23]. This is in line with the results on F. excelsior, indicating that trees with damaged crowns exhibit impaired growth [86], while those with more open crowns tend to have lower infection rates, probably due to altered microclimate conditions less conducive to fungal growth [87].

Reduced growth is a direct consequence of crown decline [32]. In the studied stand in Posavina (Serbia), the reduced vitality and decline of narrow-leaved ash trees coincided with the emergence of H. fraxinues fungus [6,7], primarily affecting trees with poor growth [23]. Thus, the natural stem exclusion cannot be eliminated as a factor in the decline process, as the species normally compete for growth space during critical development stages.

In the extensively managed stand in Posavina (Serbia), at the stand level and the predominant/dominant level, 51% were significantly defoliated in 2020, indicating a degraded stand vitality. Only 14.9% of trees were healthy (<25% defoliation, which represents the primary basis for future crop tree selection), with 41.7% being predominant/dominant trees, which is approximately 300 trees per hectare in absolute numbers. Within this number, 87 trees (29%) had free crowns. However, even apparently healthy trees may exhibit collar lesions, as observed in both F. excelsior and F. angustifolia [13,33]. Despite widespread disease, the general recommendation is to retain and support the healthy ash trees in the stand (Metzler et al., 2013, as cited by Enderle et al. [33], [39,88,89,90]). Thus, preserving the trees with undamaged crowns, even if some of them have collar lesions, may be an appropriate long-term strategy for narrow-leaved ash stands. The results of Semizer-Cumming et al. [90] suggest that such trees contribute more to generation turnover, potentially increasing the resistance of future stands. High-resolution satellite imagery may help determine stands suitable for this approach [91]. By combining appropriate silvicultural measures [39], it may be possible to enhance stand resistance and ensure the sustainability of narrow-leaved ash stands, at least on some sites.

We assume that the synergy of unfavourable abiotic and biotic factors, along with the presence of H. fraxineus, has led to a decline in the vitality of narrow-leaved ash trees in the long term. This decline is particularly evident in the studied stand in Posavina (Serbia), where the lack of thinning and phytosanitary measures during critical development stages has created an unfavourable stand structure. Our silvicultural perspective and analysis of narrow-leaved ash decline were based on the confirmed presence of H. fraxineus in the researched stand. In a complex process of tree decline [92,93], the role of the pathogen in the decline of predominant/dominant trees with free, undamaged crowns in stands with degraded vitality remains to be fully understood, requiring further investigations.

While H. fraxineus is a primary factor contributing to the defoliation of CC1 narrow-leaved ash trees, other factors, such as soil moisture and site changes, may also play a role. However, these factors were not investigated in this study, limiting our ability to fully assess their impact.

5. Conclusions

The decline of narrow-leaved ash in the studied 45–50-year-old stand on Humogley soil in Posavina (Serbia) was exacerbated by strong intraspecific competition and stem exclusion. The decline was most severe among suppressed and co-dominant trees, with a total mortality of 33.2%. Mortality among predominant/dominant trees was lower at 6.9%. Dead and dying trees of narrow-leaved ash trees, both at stand level and within the predominant/dominant crown class, exhibited smaller DBHs compared to healthy and significantly defoliated trees, suggesting that their decline is primarily linked to poor growth. In 2020, at the age of 45–50 years, 300 trees per hectare (14.9%) were classified as predominant/dominant trees with less than 25% defoliation. Among these, 87 trees had free crowns following an extensive tending management approach in the studied stand.

Our findings suggest that a silvicultural strategy focused on the timely release of predominant/dominant trees with healthy crowns from the competition may help sustain the main stand vitality in the presence of H. fraxineus.