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Article

Occurrence of European Mistletoe (Viscum album L.) on Forest Trees in Poland and Its Dynamics of Spread in the Period 2008–2018

by
Paweł Lech
1,*,
Anna Żółciak
2 and
Robert Hildebrand
1
1
Department of Forest Resources Management, Forest Research Institute, Sękocin Stary, Braci Leśnej 3, 05-090 Raszyn, Poland
2
Department of Forest Protection, Forest Research Institute, Sękocin Stary, Braci Leśnej 3, 05-090 Raszyn, Poland
*
Author to whom correspondence should be addressed.
Forests 2020, 11(1), 83; https://doi.org/10.3390/f11010083
Submission received: 11 December 2019 / Revised: 30 December 2019 / Accepted: 7 January 2020 / Published: 9 January 2020
(This article belongs to the Section Forest Ecology and Management)
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Versions Notes

Abstract

:
As recently reported, European mistletoe has become an important agent of damage to forest trees in Central Europe. To document the extent of its impact, host and environmental preferences, as well as spatial and temporal dynamics, we have analyzed the results of 10 years of annual assessments of tree damage in level 1 plots of country-wide national forest monitoring. Mistletoe was found on 12 forest tree species, most frequently on silver fir and Scots pine, much less often on birches and deciduous admixture species. Common beech, pedunculate, and sessile oaks, as well as coniferous admixture species, were found to be free from the parasite. Mistletoe was more common on larger trees, mainly those in the 1st and 2nd Kraft classes, characterized by a higher DBH value than trees without V. album. Infestation was also age-dependent with low numbers of infested trees in young age classes and a much higher proportion of infested trees being over 80–100 years in age. Defoliation of trees colonized by mistletoe was found to be significantly higher than in trees free from the parasite, confirming the adverse effect of infestation on tree health. The increase of relative incidence of tree infestation by mistletoe in forests in Poland was high throughout the entire period 2008–2018 and significant for the most threatened host species: silver fir, Scots pine, and birches. It was also found that spread direction was from west to east and that the occurrence of V. album shows clear regionalization. The most endangered forests were located within a 200 km wide zone ranging through lowland Central Poland from the border with Germany down to the border with Ukraine and Belarus. The highest concentration occurred in the Western part of the country. Outside this zone (to the north and south) the mistletoe was much less abundant as expressed by the amount of injuries caused by the parasite or infested trees per plot.

1. Introduction

European mistletoe (Viscum album L.) of the family Viscaceae (Santalaceae s.l.) [1] is an evergreen plant with functional chlorophyll, capable of fixing atmospheric carbon dioxide and, therefore, considered to be a semi-parasite (hemi-parasite) [2,3]. It penetrates the tree branches, taking up water and mineral nutrients [2,4,5] through the endophytic system which consists of the haustoria and sinkers that reach the host cambium, and cortical strands that provided lateral spread [6]. Mistletoe grows mainly on branches, and rarely on trunks of woody species [7]. The berries of V. album stick to the branch by means of the substance vascin. In Europe bird species of the Thrush family (Turdidae), e.g., the mistletoe thrush (Turdus viscivorus L.) and fieldfare (Turdus pilaris L.), the Waxwing family (Bombycillidae), e.g., Bohemian waxwing (Bombycilla garrulus L.), and Euroasian blackcap (Sylvia atricapilla L.) are considered the principal vectors of mistletoe [8,9,10,11]. These birds migrate from Africa to Europe in late winter and during this period feed on mistletoe berries [12]. Their migration paths are believed to influence the abundance of mistletoe in Central Europe [12]. The spread of mistletoe by birds, due to their preference for perching in the upper parts of taller trees, is considered to be the main reason for initially infecting the oldest and largest trees within a stand [13,14,15,16].
European mistletoe has a wide distribution in Europe and Asia and has also been introduced to North America [3,14,17]. According to Zuber [3] the European distribution area extends from 10° W to 80° E and from approximately 60° N (max. 59°38′ N) to 35° S. Mistletoe infects over 450 species and varieties of host trees [18]. According to Becker [19] some hardwood species are resistant to mistletoe infestation (e.g., Fagus sylvatica L.), while others (e.g., Quercus spp. and Ulmus spp.) are rarely infested. In dense stands mistletoe develops only on higher trees (predominant and dominant) which receive enough light [20].
The European mistletoe is divided into four subspecies with different hosts: V. album subsp. album L. on deciduous trees [3,21], V. album subsp. abietis (Wiesb.) Abromeit (white mistletoe) solely on firs (Abies spp.) [20] and V. album subsp. austriacum (Wiesb.) Vollmann is found only on pines (Pinus spp.) and spruces (Picea spp.) [3]. The fourth subspecies, V. album subsp. creticum N. Böhling, Greuter, Raus, B. Snogerup, Snogerup and Zuber grows only on Calabrian pine (Pinus brutia Ten.) and is exclusive to Crete [22].
Viscum album was recently reported by ICP Forests as an important causal agent of biotic damage to Scots and Austrian pines in Europe [23]. Similar concerns were expressed by regional reports from the Rhone valley in Switzerland [24], Brandenburg in Germany [25], Hungary [26], and Poland [27,28]. There are also publications on the occurrence of mistletoe on silver fir in France [20,29], Switzerland [30,31], Croatia [32], Romania [33], Spain [34], and Greece [35].
Mistletoes cause damage in forests, orchards, plantations, and ornamental trees worldwide. They impair host growth and vigor, reduce fruiting, wood quality and quantity, and predispose trees to attack by insects and fungi [36,37,38]. Mistletoes contribute to increased transpiration, especially in years of water deficit, and cause marked weakening of infested trees [39,40]. According to Ozturk et al. [41] mistletoe influences the anatomy of wood and needles, leading to partial or total death of the host during periods of drought [42,43], which is why it is important forest parasite. The high mortality in Scots pine stands in some places across Europe has been reported to be at least partly attributable to mistletoe infestation [24,44]. Mistletoe infection of Scots pine can be considered as both a predisposing factor for tree death by increasing needle loss, and a contributing factor by increasing water stress during drought [24]. Plagnat [29] has also reported higher mortality levels of silver fir trees infected by the mistletoe on poor, dry sites of low elevation, especially during periods of drought. According to Barbu [33,45] colonization of fir by white mistletoe also caused a significant reduction in the length of needles and premature needle drop. Bukowiec and Bednarz [46] have noticed a reduced radial growth of silver fir trees infected with mistletoe in Limanowa Forest District (Southern Poland), especially on those infested at moderate to heavy degrees. Similar findings were earlier reported by Noetzli et al. [31] from Rhine Valley (Canton of Grisons) in Switzerland.
Temperature was indicated as the limiting factor for the northern and eastern borders of V. album occurrence [47]. Mistletoe is highly temperature sensitive [48,49]. Low summer as well as low winter temperatures restrict its spread [49,50,51]. Rising average temperatures and climate change may exacerbate the spread of mistletoe to new areas. Dobbertin et al. [52] have found a 200 m upward shift of V. album occurrence in the Swiss Alps over the last 100 years.
In Poland, the most common taxon is V. album subsp. album infesting deciduous tree species, such as poplars (Populus spp.), birches (Betula spp.), maples (Acer spp.), limes (Tilia spp.), willows (Salix spp.), black locust (Robinia pseudoacacia L.), and apples (Malus spp.) [53,54,55,56,57]. The appearance of V. album subsp. austriacum (Wiesb.) Volim on Scots pine was also reported [10,16,27,28]. The range of V. album subsp. abietis is closely related to the distribution of the host silver fir (Abies alba Mill.) [53,57]. Although mistletoes have long been recorded in Poland, no country-wide attempt based on reliable data obtained through methodologically coherent observations has so far been made to determine its spatial distribution in forests and to quantify the intensity of the infection. The dynamics of pathogen spread over time have also not been determined. To fill in these gaps we have analyzed 10 years of the most recent forest monitoring data on tree damage to determine the scope of V. album occurrence in forests in Poland in relation to species of host trees, their age, diameter at breast height (DBH), social class, defoliation, and forest site type (site quality). In addition, we have investigated the parasite spread in the period 2008–2018 to identify its direction and dynamics.

2. Materials and Methods

2.1. Data

The investigation was based on the results of annual assessments of tree damage across level 1 plots of national forests monitoring in Poland between the years 2008–2018. The number of plots comprising 20 trees each ranged from 1916 in 2008 to 2023 in 2018 and the number of trees from 38,320 up to 40,460 accordingly. Plots were located in a systematic grid 8 × 8 km in forest areas all over Poland (Figure 1).
Tree injuries were evaluated visually once a year in summer (July and August) in accordance with the ICP Forests Manual, part IV: “Visual assessment of crown condition and damaging agents” [58]. The following characteristics were derived from the database and used in the analysis: tree species, age, diameter at breast height (DBH), social position, crown defoliation, and presence/absence of V. album. Forest site type within the stand compartment of the plot location was also used to determine the parasite–site relationship. It should be noted that according to national forest monitoring guidelines, a maximum of three of the most severe injuries of any kind and origin per tree were recorded, even when there were more of them present. In consequence our estimates of the incidence of V. album are likely conservative.

2.2. Methods of Analysis

To evaluate mistletoe infestation intensity the parameter reflecting the number of damages caused by V. album per tree was used. It was determined in accordance with the following formula:
F = 100 n/N
where:
  • F—coefficient of V. album appearance frequency;
  • n—number of injuries caused by V. album on trees of a given species or all species together; and
  • N—total number of trees of a given species or all species together.
The formula allows to make comparisons between groups of trees selected in different tree and site categories.
To evaluate the trends over time the Mann–Kendall test was applied. It was used to identify the direction of change of frequency of appearance of V. album (F coefficient) in the period 2008–2018 (i.e., increase, decrease, no trend) and to check its significance. Another test used to analyze the frequency data was the χ2 test for independence which was applied to identify the relationship between the age of trees or their social position and the mistletoe infestation of the tree. This kind of analysis was also used to determine the parasite preferences for site quality (fertility, water availability, and elevation). Finally, the averages of DBH and tree defoliation scores for trees infested and not infested by mistletoe were compared with the use of Student’s t-test. A modified version of the test was used in the case of unequal variances, as occurred when comparing defoliation means of all species, Scots pine, and silver fir. It should be also mentioned that in the case of trend analysis data from the entire period 2008–2018 was utilized while for other tests only data from 2018 was analyzed. Data from trees in plots where mistletoe was recorded was used for analysis with such parameters as DBH, social position, and defoliation, while data from the entire 2018 dataset was used for age and site quality. The cross-tabulation, χ2 and Student’s t-tests were performed with the use of commercial software package Statgraphics Centurion XV [59] and trend analysis with the R v.3.6.0, package Kendall [60,61].

3. Results

3.1. Mistletoe Occurrence on Tree Species

In the years 2008–2018 mistletoe was identified as a cause of injuries on the following 12 forest tree species: Scots pine (Pinus sylvestris L.), silver fir (Abies alba Mill.), silver birch (Betula pendula Roth), downy birch (B. pubescens Ehrh.), black alder (Alnus glutinosa Gaertn.), and on admixture deciduous species, such as maple (Acer platanoides L.), ash (Fraxinus excelsior L.), black locust (Robinia pseudoacacia L.), white poplar (Populus alba L.), aspen (P. tremula L.), black poplar (P. nigra L.), and small-leaved lime (Tilia cordata Mill.). However the proportion of mistletoe among distinguished causative damage factors was relatively small. In 2018 the parasite was the cause of just 615 injuries, which accounted for 1.3% of all registered tree injuries and appeared on 606 trees (1.5% of all trees subjected damage assessment). In previous years recorded injuries caused by V. album were even fewer, starting with 38 in 2008, 207 in 2012, and 407 in 2016 (Table 1).
In 2018 V. album occurred most frequently on silver fir (F = 3.46) and Scots pine (F = 2.35), with one damage symptom caused by V. album present on every 29th and 43rd tree of these species, respectively. Significantly lower values of the coefficient characterized birches (F = 0.97) and admixture deciduous species (F = 0.56) (Table 1). Species free from injuries caused by mistletoe were Norway spruce, admixture conifers (mainly larch), oaks, and common beech. It should be noted that, in 2008, V. album was found only on Scots pine and silver birch. In subsequent years, it was also identified as a causal agent of damages of other tree species, such as silver fir and admixture deciduous species (from 2010 to the end of the analyzed period). It also occurred on black alder from 2013–2016 but on very few trees.

3.2. Spatial and Temporal Dynamics of Mistletoe Spread

Despite a relatively low number of injuries caused by mistletoe, a significant increase of the F coefficient was observed throughout the entire study period 2008–2018, especially for the most affected species: Scots pine, silver fir and birches, as indicated by the Mann–Kendall trend test. For less frequently infested group of species, i.e., the admixture deciduous species, the increase was not significant (Table 1). The highest relative increase in number of injuries caused by mistletoe occurred in 2010, 2012, and 2018 (Figure 2).
For these years the increases were close to or exceeded 50% of the number of mistletoe counts of the previous year. Significant and rapid increase in the number of injuries caused by V. album in the period 2008–2018 was accompanied by a similar increase of number of plots with trees affected by the parasite. In 2008 the mistletoe was present on just 18 level 1 plots located mostly in the western part of the country, while in 2018 it was found on 179 plots distributed over a much greater area, covering a zone in the central lowland part of Poland from the west to the east and accompanied by secluded plots with the parasite located mainly in Eastern Poland (Figure 3).
This indicates that the spatial distribution of plots with mistletoe showed significant regionalization. Regions with the highest share of plots with the parasite were found in the Lubusz region (west of the country), Southern Greater Poland, Northern Silesia, Southern Mazovia, and Northern Lower Poland. In contrast there were large areas in which V. album was not found on forest trees at all or where it was very rare. These areas include the south of Poland, in the Sudety and Carpathian Mountains along the border with the Czech Republic and Slovakia, as well as in the northern part of Poland. Within the period 2008–2018 the spatial pattern of the parasite spread proceeded from west to east and increased in frequency of occurrence within plots. In 2009 the maximum number of injuries caused by mistletoe that occurred on single plot was five while in 2012 there were six plots with 10 or more such tree injuries, in 2015—10 plots and in 2018—13 plots.

3.3. Mistletoe Occurrence in Relation to Age Classes of Trees

In 2018 the occurrence of V. album on Scots pine, common fir and birches as well as on all species together showed a significant dependence on the age of trees. The lowest values of the F coefficient were found for the youngest age class (21–40 years of age), then rose gradually and reached the highest scores for the oldest trees—over 120 years of age in the case of Scots pine, common fir, and all species together, and 81–100 years for birches (Figure 4). In these particular age classes, mistletoe occurred on every 8th Scots pine, 11th silver fir, and 28th birch tree.

3.4. Mistletoe Occurrence in Relation to Site Condition

The V. album occurrence in relation to site condition considered three features of the plot location: soil fertility, water availability (soil moisture), and site elevation. The following fertility classes were determined in accordance to their suitability for tree species: coniferous—low fertility sites, coniferous-mixed—low to medium fertility sites, deciduous-mixed—medium to high fertility sites and deciduous—high fertility sites. In the case of Scots pine and birches the proportion of trees with mistletoe was lowest on highly fertile (deciduous suitable) sites, but differences between sites were significant for Scots pine only (Figure 5). Viscum album occurring on silver fir was recorded on medium to high and highly fertile sites with very small differences between these two fertility classes and was completely absent in poor soils due to the lack of fir trees on those sites. The highest share of Scots pine trees with mistletoe was found on medium to highly fertile sites and of birches on low to medium fertility sites.
Significant differences in the percentage of trees infested by mistletoe among site moisture classes (dry, fresh, moist and very moist) were found in the case of Scots pine only (Figure 6). The incidence of mistletoe was greatest on dry sites (11.11% of trees), 3–4 times higher than on the fresh and moist sites and 17 times more than in very wet ones. However, these results should be treated with caution because only three plots were located on dry sites with 45 pines of which five of them were found to be injured by mistletoe. In the case of silver fir and birches, differences between moisture classes were small and insignificant, with the largest percentage of trees attacked by V. album in very moist sites.
The highest percentage of Scots pines inhabited by V. album (2.51%) was on lowland locations, while much smaller on the upland sites—0.69% of trees with mistletoe (Figure 7). The parasite was not found on any of the 305 pines growing on mountain sites. In the case of silver fir, the highest percentage of infested trees was found on plots in upland locations (5.75%) and significantly less on mountain and lowland sites (1.93% and 1.04% of trees with mistletoe, respectively). In the case of pine and fir, the significance of variability of tree colonization by V. album among elevation categories was confirmed. Mistletoe occurrence on birches was independent of site elevation, but infected trees were found only on lowland sites (0.86% of trees with mistletoe), while in upland and mountain locations birches were free from the parasite (Figure 7).

3.5. Mistletoe Occurrence in Relation to Size of Tree

Occurrence of mistletoe in relation to the size of the tree was analyzed with the use of two features: social position within the stand according to Kraft classification (class 1—predominant trees, class 2—dominant trees, class 3—subdominant trees, class 4—suppressed trees and class 5—dying trees) and diameter at breast height (DBH). The analysis was limited only to trees growing on the plots on which the V. album was present.
The incidence of mistletoe infection was significantly associated with social position of trees for Scots pine, silver fir and all species combined, but not for birches (Figure 8). The proportion of trees with injuries caused by V. album was greatest for trees in Kraft class 1 (over 33% of trees), while in the class 5 trees with mistletoe were not present at all. Scots pines and silver firs from Kraft class 2 were characterized by a lower percentage of trees attacked by the parasite (25.4% and 30.8%, respectively), followed by trees from class 3 (12.2% and 13.3%). Scots pine was also the only species in which trees from the 4th Kraft class were found to be infested by V. album, however, their percentage was small with only 5.3% of trees from this class affected (Figure 8).
In addition, the mean DBH of trees with mistletoe was significantly greater than that of trees without the parasite for all distinguished tree species and trees altogether (Figure 9). In the case of birches DBH difference was found to be of slight significance (p = 0.055).

3.6. Effect of Mistletoe Infestation on Health Condition of Trees

Tree crown defoliation was used as an indicator of trees’ health status. For all indicated species and trees altogether infested specimens had higher defoliation levels than those not attacked by the parasite (Figure 10). For silver fir the difference was very small and not significant, while birches had the largest difference, although it was still only slightly significant (p = 0.050). The reason for this might be the low number of trees with mistletoe, as for each of these species only 31 trees were infested.

4. Discussion

Recent publications on the topic of V. album occurrence in forests in Poland [27,28] are based on a single-year evaluation (for 2018) that was limited to Scots pine stands managed by State Forest Holding only. However the results presented reflect quite accurately the current state of parasite abundance and endangerment caused by mistletoe to the Scots pine stands in the country. Our study has confirmed these findings.
Forest monitoring data on damages caused by V. album are currently the only available source of country-wide, reliable information on parasite occurrence on forest trees in Poland. Data has been collected for 10 years with methodologically coherent, annual observations, accompanied by various site, stand, and tree variables. The data now enables the determination of the spatial extent and temporal dynamics of mistletoe, as well as the parasite relationship with certain environmental conditions, host species, size of trees, and its effect on tree health status. However, the methodology of forest heath monitoring might have affected the results obtained. First, damage assessment is performed in the summer (July and August), at the time of maximum foliage development. Due to the limited visibility of upper parts of tree crowns at this time of year it is sometimes difficult to identify the presence of mistletoe, especially in the early stages of parasite development. Additionally, a full extension of understory vegetation limits the tree crown visibility in many plots, which also makes finding mistletoe more difficult. Another limitation comes from reporting no more than three injuries per tree. In the case of a severely affected specimen, the 4th, 5th, and next injuries are simply omitted. This is why the reported number of trees infested by mistletoe (606 specimens in 2018) should be considered as significantly underestimated. Without special research dedicated solely to the assessment of V. album in forests, more accurate results could not be obtained. Nevertheless, it was possible to identify 12 tree species occurring as hosts of V. album in forests in Poland. They included species of high importance to the country’s forests, such as Scots pine, silver fir, silver birch, as well as admixture deciduous species (maples, ash, lime, poplars, black locust). The three mistletoe subspecies (V. album subsp. album, subsp. abietis, and subsp. austriacum) were, thus, confirmed in affecting forest trees in Poland, as was earlier indicated by Stypiński [10]. It was also found that certain species were not infested by the parasite, such as Norway spruce, oaks native to Poland, beech, and admixture conifers.
Our research documented the relationship between the incidence of mistletoe and the age of trees, their size, and social position within the stand. We found that V. album occurred mainly on larger diameter trees from the upper layers of the stand (predominant and dominant) and on the oldest trees, these being Scots pine and silver fir over 120 years of age and birches 80–100 years of age. These results agreed with those from previous studies [13,14,15,16,20]. We also analyzed the incidence of the parasite and its association with forest site conditions, such as soil fertility, water availability, and elevation. Although the results on these issues are not clear and need further study, we found that different mistletoe subspecies had different site requirements. For example V. album subsp. austriacum, the parasite of Scots pine, most often occurred on trees growing on dry and poor sites located on lowlands, while V. album subsp. abietis infects silver fir on trees found in fertile and very moist soils occurring on uplands. This means that V. album subspecies’ preferences are basically the consequence of habitat requirements of their hosts. Similar conclusions were presented by Zuber [3].
Changes in the spatial distribution and temporal occurrence of V. album in Poland have been highly dynamic in the years 2008–2018. Although there is no adequate Polish publication enabling comparison, results from other Central European countries and regions were similar. A rapid increase in tree injuries caused by mistletoe were reported in recent years from Switzerland, Brandenburg in Germany, Hungary, and Romania [24,25,26,33]. In addition the last ICP Forests 2018 Technical Report indicated, for the first time, the high importance of mistletoe as a causative agent of biotic damages to Scots and Austrian pines [23]. The spatial distribution of V. album in Poland in 2018 has shown clear regionalism, with the highest concentration of the parasite on plots located in Western and Central Poland, adjacent to Brandenburg, and lowest in the northern part of the country and in the mountains in the south. This corresponds to the spatial pattern of drought events observed periodically in recent years in Poland [62,63], with the highest severity in the areas with the strongest mistletoe presence. It is in line with numerous publications linking the spread of mistletoe occurrence with climate change and global warming in recent decades [3,49,52]. This might be a consequence of the strong dependence of V. album on temperature acting as a limiting factor on its occurrence [47,50] due to the sensitivity of the parasite to low temperatures [48,49].
According to Rigling et al. [64] and Dobbertin et al. [24,44] in seasonally dry sites, host trees of P. sylvestris severely infested by V. album show crown defoliation, leading to the reduction of radial-growth rates and vitality. We have also found that defoliation of trees infested by mistletoe was significantly higher than in trees free from the parasite, especially in the cases of such tree species as Scots pine and birches. The difference in the case of silver fir trees at level 1 monitoring plots in Poland was insignificant, which is opposite to findings regarding this tree species by Oliva and Colinas [34], Diminić et al. [65], and Barbu [66]. These researchers have reported a positive relationship between crown defoliation and the intensity of mistletoe infestation.

5. Conclusions

The study presents for the first time the analyses results of data on the occurrence of European mistletoe during last 10 years from all forests in Poland, regardless of ownership, age, species structure, or composition. It allowed us to draw conclusions regarding V. album occurrence and spread in Poland and its relationship with host species, tree age, and size, as well as site condition. We have found that:
■
The occurrence of mistletoe increased continuously throughout the entire period of 2008–2018.
■
The highest concentration of parasite infestation was found in Western and Central Poland, gradually spreading to the East.
■
Viscum album was found on 12 forest tree species confirming presence of three subspecies (subsp. album, subsp. austriacum, and subsp. abietis) in forests in Poland. Tree species with the highest infestation rates were silver fir, Scots pine, and birches.
■
The oldest and biggest trees (predominant and dominant) were infested most frequently.
■
Defoliation of trees infested by mistletoe was higher than in trees free from the parasite.
■
The methodology of damage assessment used in forest monitoring may underestimate of mistletoe identification and endangerment to trees.
■
Warm and dry conditions of vegetation period and mild winter months may have contributed to the spread of mistletoe in Polish forests in recent years.

Author Contributions

Data curation: P.L. and R.H.; formal analysis: P.L.; investigation: P.L.; methodology: P.L.; project administration: P.L.; visualization: P.L. and R.H.; writing—original draft: P.L. and A.Ż.; writing—review and editing: P.L., A.Ż., and R.H. All authors have read and agreed to the published version of the manuscript.

Funding

This paper was partially supported by the Chief Inspectorate of Environmental Protection (GIOŚ) and the State Forest Holding (DGLP) in Poland through numerous projects enabling collection of monitoring data on forest health condition in the period 2008–2018.

Acknowledgments

The authors thank the Chief Inspectorate of Environmental Protection (GIOŚ) and the State Forest Holding (DGLP) for raw data, Joanna Ukalska for assistance in statistical analysis of data and the anonymous reviewers for their valuable comments and suggestions.

Conflicts of Interest

Authors declare no personal circumstances or interests that may be perceived as inappropriately influencing the representation or interpretation of reported research results.

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Figure 1. Location of forest monitoring level 1 plots in Poland.
Figure 1. Location of forest monitoring level 1 plots in Poland.
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Figure 2. Number of injuries caused by mistletoe and its relative increase in the period 2008–2018.
Figure 2. Number of injuries caused by mistletoe and its relative increase in the period 2008–2018.
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Figure 3. The occurrence of tree injuries caused by mistletoe on the forest monitoring level 1 plots in Poland in 2009, 2012, 2015, and in 2018.
Figure 3. The occurrence of tree injuries caused by mistletoe on the forest monitoring level 1 plots in Poland in 2009, 2012, 2015, and in 2018.
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Figure 4. Percentage of trees with injuries caused by mistletoe in relation to 20 years age classes of trees, and the results of the χ2 test for independence for all trees together (all species), and separately for species most infested by mistletoe (Scots pine, silver fir and birches).
Figure 4. Percentage of trees with injuries caused by mistletoe in relation to 20 years age classes of trees, and the results of the χ2 test for independence for all trees together (all species), and separately for species most infested by mistletoe (Scots pine, silver fir and birches).
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Figure 5. Percentage of trees with injuries caused by mistletoe in relation to fertility of sites, where the plots were located, and the results of the χi2 test for independence for all trees together (all species) and separately for species most infested by mistletoe (Scots pine, silver fir and birches).
Figure 5. Percentage of trees with injuries caused by mistletoe in relation to fertility of sites, where the plots were located, and the results of the χi2 test for independence for all trees together (all species) and separately for species most infested by mistletoe (Scots pine, silver fir and birches).
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Figure 6. Percentage of trees with injuries caused by mistletoe in relation to water availability on sites, where the plots were located, and the results of the χ2 test for independence for all trees together (all species) and separately for species most infested by mistletoe (Scots pine, silver fir, and birches).
Figure 6. Percentage of trees with injuries caused by mistletoe in relation to water availability on sites, where the plots were located, and the results of the χ2 test for independence for all trees together (all species) and separately for species most infested by mistletoe (Scots pine, silver fir, and birches).
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Figure 7. Percentage of trees with injuries caused by mistletoe in relation to elevation above sea level of sites were the plots were located and the results of the χ2 test for independence for all trees together (all species) and separately for species most infested by mistletoe (Scots pine, silver fir, and birches).
Figure 7. Percentage of trees with injuries caused by mistletoe in relation to elevation above sea level of sites were the plots were located and the results of the χ2 test for independence for all trees together (all species) and separately for species most infested by mistletoe (Scots pine, silver fir, and birches).
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Figure 8. Percentage of trees with injuries caused by mistletoe in relation to social position (Kraft classes) of trees and the results of the χ2 test for independence for all trees together (all species) and separately for species most infested by mistletoe (Scots pine, silver fir, and birches).
Figure 8. Percentage of trees with injuries caused by mistletoe in relation to social position (Kraft classes) of trees and the results of the χ2 test for independence for all trees together (all species) and separately for species most infested by mistletoe (Scots pine, silver fir, and birches).
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Figure 9. The average DBH of trees attacked by V. album and free from the parasite on the plots with mistletoe present and the results of the Student’s t-test where “ab” denotes a significant difference between means (p < 0.05) and “a*b*” denotes slight significance (p = 0.055).
Figure 9. The average DBH of trees attacked by V. album and free from the parasite on the plots with mistletoe present and the results of the Student’s t-test where “ab” denotes a significant difference between means (p < 0.05) and “a*b*” denotes slight significance (p = 0.055).
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Figure 10. Average percentage defoliation of trees attacked by V. album and free from the parasite in the plots with mistletoe present, and the results of the Student’s t-test where “ab” denotes significant difference between the means (p ≤ 0.05), “aa”—not significant difference between means (p > 0.05).
Figure 10. Average percentage defoliation of trees attacked by V. album and free from the parasite in the plots with mistletoe present, and the results of the Student’s t-test where “ab” denotes significant difference between the means (p ≤ 0.05), “aa”—not significant difference between means (p > 0.05).
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Table
Table 1. Mistletoe occurrence on major Poland forest tree species and groups of species in forest monitoring level 1 plots in the years 2008–2018 in Poland as expressed by the absolute number of tree injuries caused by V. album, the F coefficient, and the trend determined by the Mann–Kendall test.
Table 1. Mistletoe occurrence on major Poland forest tree species and groups of species in forest monitoring level 1 plots in the years 2008–2018 in Poland as expressed by the absolute number of tree injuries caused by V. album, the F coefficient, and the trend determined by the Mann–Kendall test.
YearUnit/CoefficientScots PineSilver FirBirchesBlack AlderOther DeciduousTotal
2008count29 5 438
F0.13 0.13 0.220.07
2009count3847 453
F0.170.420.18 0.180.14
2010count110815 2135
F0.490.830.38 0.080.35
2011count1111013 6140
F0.501.050.33 0.240.36
2012count182118 6207
F0.821.120.20 0.240.53
2013count213115319251
F0.961.110.120.120.740.64
2014count2501315225305
F1.111.310.350.080.940.76
2015count2831623113336
F1.251.600.540.040.480.84
2016count3372027122407
F1.511.970.640.040.821.02
2017count3632129 16429
F1.632.020.67 0.581.07
2018count5213642 16615
F2.353.460.97 0.561.52
M–K trendIII PII
I—increase; PI—probable increase.

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Lech, P.; Żółciak, A.; Hildebrand, R. Occurrence of European Mistletoe (Viscum album L.) on Forest Trees in Poland and Its Dynamics of Spread in the Period 2008–2018. Forests 2020, 11, 83. https://doi.org/10.3390/f11010083

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Lech P, Żółciak A, Hildebrand R. Occurrence of European Mistletoe (Viscum album L.) on Forest Trees in Poland and Its Dynamics of Spread in the Period 2008–2018. Forests. 2020; 11(1):83. https://doi.org/10.3390/f11010083

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Lech, Paweł, Anna Żółciak, and Robert Hildebrand. 2020. "Occurrence of European Mistletoe (Viscum album L.) on Forest Trees in Poland and Its Dynamics of Spread in the Period 2008–2018" Forests 11, no. 1: 83. https://doi.org/10.3390/f11010083

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