Schlüsselbegriffe: Dürre, weißbeerige Mistel, Waldphytopathologie, Pflanzenparasiten, Waldkiefer, Tschechische Republik
Abstract
The infection rate (assigned in classes 0–6) of European mistletoe (Viscum album subsp. austriacum [Wiesb.] Vollm.) on Scots pine (Pinus sylvestris L.) in the Czech Republic was analysed from May 2019 to June 2020 in relation to Forest Infrared Index (FII: low, high), stand age (21–50, 51–70 and 71–90 years), tree position (at stand edge, within stand), stem diameter at breast height (DBH) and defoliation (0–10%, > 10–25%, > 25–60% and > 60–99%) in five natural forest areas (NFA). In each NFA, the analysis were done at two locations, one with a low FII and one with a high FII. At each locality and in each of the three stand age categories, the DBH, defoliation and mistletoe infection rate were assessed for 25 trees in the stand edge and 25 trees within the stand. Statistically significant higher mistletoe infection rate was recorded in stands with high FII (higher drought stress), in older stands (highest for 71–90 years followed by 51–70 years) and on trees at the stand edge, that have higher DBH and higher defoliation (highest for > 60–99% followed by > 25–60% and lowest for > 10–25%). The differences between NFAs were also significant. Our results suggest, that (1) selecting drought- and heat-resistant P. sylvestris varieties, (2) focussing plantation efforts to areas with lower temperatures and higher precipitation and (3) the reduction of the rotation period are recommended for Pinus sylvestris forest management in Central Europe.
Zusammenfassung
Der Befall (eingeteilt in Klassen 0–6) der Kiefern-Mistel (Viscum album subsp. austriacum [Wiesb.] Vollm.) auf der Waldkiefer (Pinus sylvestris L.) wurde im Zeitraum Mai 2019–Juni 2020 analysiert für 5 natürliche Waldbestände (NFAs) hinsichtlich des Infrarotindex des Waldes (FII: niedrig, hoch), der Altersklasse (21–50, 51–70, 71–90 Jahre), der Position im Bestand (am Bestandesrand, innerhalb des Bestandes), dem Stammdurchmesser in Brusthöhe (DBH) und der Kronenverlichtung (Defoliation, 0–10%, > 10–25%, > 25–60% und > 60–99%). In jedem NFA wurde die Auswertung in einem Gebiet mit niedrigem FII sowie einem mit hohem FII durchgeführt. An jeder Lokalität wurden innerhalb jeder der drei Altersklassen an 25 Bäumen am Rand und an 25 Bäumen in Bestandesinneren der DBH, Kronenverlichtung und Mistelbefall gemessen. Ein statistisch signifikant höherer Mistelbefall wurde in Beständen mit hohem FII (höherer Stress durch Trockenheit), in älteren Beständen (am stärksten in Beständen mit 71–90 Jahre, gefolgt von Kategorie 51–70 Jahre), an Bäumen am Rand des Bestandes, mit einem höheren DBH und einer höheren Kronenverlichtung festgestellt. Der Einfluss der NFAs war ebenfalls statistisch signifikant. Die Ergebnisse dieser Studie legen folgende Maßnahmen zur Bewirtschaftung von Waldkiefernbeständen in Mitteleuropa nahe: (1) Einsatz von trockenheitsresistenten Waldkiefer Sorten, (2) Fokussierung des Anbaus in kühleren und niederschlagsreicheren Gebieten und (3) Verkürzung der Umtriebszeit.
1 Introduction
European mistletoe (Viscum album L.) is a dioecious, evergreen, hemi-parasitic plant from the family Santalaceae. Viscum album is insect pollinated. The white fleshy berries are eaten and dispersed by birds, the most important are the mistle thrush (Turdus viscivorus L.), fieldfare (Turdus pilaris L.), Bohemian waxwing (Bombycilla garrulous L.) and Eurasian blackcap (Sylvia atricapilla L.) (Zuber 2004). Viscum album grows on stems and branches of woody plants, from which it drains water and inorganic compounds. Mistletoe haustorial system cause tubular corridors in the host's wood, leading to the technical degradation of the wood (Příhoda 1959). Woody plants heavily infested with mistletoe show reduced radial growth (Noetzli et al. 2003; Barbu 2009; Rigling et al. 2010; Sangüeesa-Barreda et al. 2013; Pilichowski et al. 2018; Bilgili et al. 2018). On Scots pine (Pinus sylvestris L.), Viscum album infection can lead to crown degradation in its host, reduction in primary production, decrease in carbohydrate availability (Rigling et al. 2010), reduction in needle length, weight (Mutlu et al. 2016b; Bilgili et al. 2020a), area and width (Bilgili et al. 2020a), reduction of nitrogen content in needles (Galiano et al. 2011), reduction of size and mass of the cones, the number and weight of seeds, and the height and weight of the seedlings (Jasiczek et al. 2017). The degrading crown have reduced the length, the radial increment, the ramification, and the number of needle years of the infested branches (Rigling et al. 2010). Viscum album infection on P. sylvestris affects both the host’s anti-oxidative defense system and the phytohormone profile after establishment of the xylem tapping haustorium (Hu et al. 2017) and causes inhibition of chlorophyll (Mutlu et al. 2016b). Hosts heavily infested with mistletoe may die (Noetzli et al. 2003; Mutlu et al. 2016a). Mistletoe is a serious threat for host trees, especially during drought periods, because it increases their hydric stress by draining water (Dobbertin and Rigling 2006; Rigling et al. 2010; Mutlu et al. 2016b), decreaces the availabitity of nutrients (Mutlu et al. 2016b) and increases their risk of bark beetle infestation (Tsopelas et al. 2004). Mistletoe-induced stomatal closure is a successful mechanism of the hosts against dying from hydraulic failure in the short term but increases the risk of carbon starvation in the long term (Zweifel et al. 2011). Viscum album produces viscotoxins, small proteins with three reducible disulfide bonds. The most abundant Viscum album subsp. austriacum viscotoxin (1-PS) is positively correlated with summer precipitation and autumn irradiance ratios, and negatively correlated with the host´s leaf nitrogen and sulfur status (Seegmueller 2012).
Hosts of Viscum album include over 150 genera, and the genus Pinus is a common host (Barney et al. 1998). Viscum album includes several subspecies, differing in habitat and the hosts. Three of the subspecies occur in the Czech Republic. Viscum album L. subsp. album attacks deciduous trees, especially Malus spp., Populus spp., Tilia spp., Acer spp., and Pyrus spp., Sorbus spp., Jungans spp., Quercus spp. and Robinia spp. (Zuber 2004; Box 2019; EPPO 2021). Viscum album subsp. abietis (Wiesb.) Abrom. with broad green leaves occurs only on firs (Abies spp.) (Zuber 2004; EPPO 2021). Viscum album subsp. austriacum (Wiesb.) Vollm. with narrow yellow-green leaves parasitizes conifers, especially on Pinus spp., including P. sylvestris and Austrian pine (P. nigra J.F. Arnold) (Zuber 2004; Box 2019; EPPO 2021), but it may also occurs on Larix spp. and Picea spp. (Zuber 2004; Schrack and Döring 2004; EPPO 2021).
Viscum album naturally occurs in Europe, mostly in the lowlands and hilly areas, but it is absent in many areas (especially those with high altitudes). In recent decades, there has been a marked increase in the occurrence of all Viscum album subspecies on both forest and non-forest trees (Dobbertin et al. 2005). In Poland, the occurrence of Viscum album increased continuously throughout the period of 2008–2018, the most on P. sylvestris, silver fir (Abies alba Mill.) and white birch (Betula pendula Roth) (Lech et al. 2020). In P. sylvestris forest in southeast Berlin (Germany), approximately 25% reduction in basal area increment of trees during the last 9 years of heavy infection of Viscum album (Kollas et al. 2017). In many dry inner-Alpine valleys, the increasing mistletoe abundance was reported to accelerate the ongoing pine decline (Zweifel et al. 2011). In the Klagenfurt (Austria), Viscum album subsp. album has been recorded on various deciduous trees for the first time (Leute and Perko 1999). In Hungary, the area infested by Viscum album has almost tripled since the beginning of the 20th century (Varga et al. 2014). The increase in the occurrence of Viscum album is probably due to long-term high temperatures. If these weather conditions persist, Viscum album can be expected to continue to spread to higher altitudes and to be an increasingly important factor involved in the decline and mortality of individual trees and entire stands, including pine stands (Dobbertin et al. 2005).
Pruning and tree removal are the primary control measurements for Viscum album (Butin 1995). However, thinning favors the growth of Viscum album by increasing light levels in thinned stands (Noetzli et al. 2003). Mistletoe shoots can be broken off or cut off, but due to new sprout growth from the cortical haustoria it must be done repeatedly. Effective chemical preparations against Viscum album are growth regulators, which can be used while the host is dormant (Sinclair and Lyon 2005). The hosts most susceptible to Viscum album infection can be replaced by more resistant species, e. g. Norway spruce (Picea abies [L.] H. Karst.) or European beech (Fagus sylvatica L.), or by more resistant cultivars (Noetzli et al. 2003; Zuber 2004). The aims of this study were: 1) to evaluate the occurrence of Viscum album subsp. austriacum on P. sylvestris stands in the areas of highest occurrence of Viscum album subsp. austriacum in the Czech Republic based on the Forest Infrared Index (FII), stand age, tree position in the stand, defoliation and stem diameter at breast height (DBH) in five natural forest areas, 2) to assess which factors are related to Viscum album infection and 3) to formulate management recommendation for the protection and management of P. sylvestris stands against Viscum album infection in the climatic conditions of the Central Europe.
2 Materials and methods
From May 2019 to June 2020, one-time evaluations of Viscum album infection rates on P. sylvestris trees in forest stands in the Czech Republic were conducted. Natural forest areas (NFAs) in the Czech Republic have been established based on geological, climatic, orographic and phytogeographical conditions (ÚHÚL 2021). We selected five NFAs with an abundance of P. sylvestris (Figure 1). These were Západočeská pahorkatina, Středočeská pahorkatina, Jihočeské pánve–část Třeboňská pánev, Polabí, Jihomoravské úvaly (Figure 2). Predisposition to Viscum album infection rate due to drought stress was evaluated using the forest infrared index (FII), which has been established as a basic indicator of forest health. FII is defined as the normalized ratio of water content to the state of the cellular structure of the assimilation apparatus in the stand. A higher FII means a worse state of cell structure and lower water content in the assimilation apparatus (ÚHÚL 2021). The FII values were obtained from the Map Information Catalog. The FII values from the catalog for year 2017 were used (ÚHÚL 2021), as maps with FII for years 2019–2020 were not available. At each NFA, one locality with a low FII and one locality with a high FII were studied (Table 1). At each locality, three stands were evaluated according to their ages: 20–50 years, 51–70 years and 71–90 years. Stands less than 20 years (due to minimal or no infection by mistletoe) and trees with ages, that did not correspond with the stand age, were excluded from the analysis. In each stand, 25 trees along the stand edge were measured. Theses trees were adjacent to each other, hence no tree along the stand edge was left out until 25 trees were measure. Likewise, we measured 25 trees within the stand, along a line dividing the stand into two approximately equal parts, using a compass. The stem diameter of each tree was measured at a height of 1.3 m above ground (DBH) using a forest calliper with an accuracy of 0.5 cm. Percentage defoliation of each tree was estimated in 5% steps and then assigned to one of four categories: 0–10%, > 10–25%, > 25–60% or > 60–99% (CEC-UN/ECE 1993). Dead trees (100% defoliation) were excluded from the analysis. For this reason, the number of sampled trees was lower than 25 in some stands (especially at locality Čelina; Table 1). The Viscum album infection rate of each tree was evaluated using the internationally recognized six-class dwarf mistletoe rating system (Hawksworth 1977). This rating system was developed for lodgepole pine dwarf mistletoe (Arceuthobium americanum Nutt. ex Engelm.), but it has already been successfully used to evaluate infection rates of Viscum album on Greek fir (Abies cephalonica Loudon) (Tsopelas et al. 2004), and on P. sylvestris (Bilgili et al. 2018; Bilgili et al. 2020b). The tree crown was visually divided into three equal parts. Each third was rated 0 for no mistletoe infection, 1 for light mistletoe infection (less than 50% of the branches infected) or 2 for heavy mistletoe infection (50% or more of the branches or stem infected). The ratings of the three parts were summed to obtain a total value for the whole tree (ranging from 0–6) (Hawksworth 1977; Figure 3).
© Table 1: Summary information for all research plots. NFA – natural forest area; FII – Forest Infrared Index; Age – stand age (years); Position – tree position in the stand; DBH (cm) – diameter at breast height (cm); Viscum album – Viscum album subsp. austriacum infection rate (values 0-6); N – number of sampled trees. We show arithmetic mean plus-minus Standard Deviation (SD). / Tabelle 1: Zusammenfassung für alle Untersuchungsflächen. NFA – natürliches Waldgebiet; FII – Infrarotindex des Waldes; Age – Alter des Bestands; Position – Position des Baumes im Bestand; DBH – Brusthöhendurchmesser; Viscum-Album-Infektionsrate (Werte 0–6); N – Anzahl der beprobten Bäume. Wir zeigen arithmetische Mittelwert plus-minus Standardabweichung.
Table 2: Generalized linear model (GLM) of Viscum album subsp. austriacum infection rate.Total number of observations were 1470. Effect – tested variables, df – degrees of freedom, Wald – value of the Wald Chi-square test, p – significance level (* P < 0.05 *** P < 0.001), NFA – natural forest area, FII – Forest Infrared Index, Age – stand age, Position – tree position in the stand, Defoliation – percentage tree defoliation, DBH – diameter at breast height. / Tabelle 2: Verallgemeinertes lineares Modell (GLM) des Mistelbefalls. Anzahl der Beobachtungen ist 1470. Effect – getestete Variable, df – Freiheitsgrade, Wald – Wert des Wald-Chi-Quadrat-Tests; P – Signifikanzniveau (* p < 0.05 *** p < 0.001); NFA – natürliches Waldgebiet; FII – Infrarotindex des Waldes; Age – Alter des Bestands; Position – Position des Baumes im Bestand; Defoliation – prozentuelle Kronenverlichtung der Bäume; DBH – Brusthöhendurchmesser.
A statistical evaluation for the whole trees was performed using SPSS Statistics Version 27 software from the IBM company. A generalized linear model (GLM) was used to test the significance of the predictors (NFA, FII, stand age, tree position in the stand, defoliation and DBH) to Viscum album infection rate (Denis 2019) (Table 2). Differences between the Viscum album occurrence (0–2) in crown thirds (upper, middle, lower was analysed with Kruskal-Wallis and subsequent pairwise Dunn's tests was performed using Statistica 10 from StatSoft company.
3 Results
Figure 4: Box plots of Viscum album infection rate (range of values 0–6) for natural forest areas (NFA), the Forest Infrared Index (FII), stand age, tree position in the stand, defoliation and diameter at breast height (DBH). Center line – arithmetic mean, box – standard deviation. NFAs: 6 – Západočeská pahorkatina, 10 – Středočeská pahorkatina, 15b – Jihočeské pánve – část Třeboňská pánev, 17 – Polabí, 35 – Jihomoravské úvaly. N – number of observations. / Abbildung 4: Boxplot des Viscum-album-Befalls (Wertebereich 0–6) für natürliche Waldbestände (NFA), zum Infrarotindex des Waldes (FII), zum Alter des Bestandes, zur Position des Baumes im Bestand, zur Defoliation und zum Brusthöhendurchmesser (DBH). Mittelstrich – arithmetisches Mittel, Kasten – Standardabweichung, NFAs: 6 – Západočeská pahorkatina, 10 – Středočeská pahorkatina, 15b – Jihočeské pánve – část Třeboňská pánev, 17 – Polabí, 35 – Jihomoravské úvaly. N – Anzahl der Beobachtungen.
The Viscum album subsp. austriacum infection rate differed statistically significantly between NFA (Table 1). We observed the highest infection rate in NFA Jihomoravské úvaly and the lowest in NFA 10 Středočeská pahorkatina, but the differences between individual NFAs were not significant (Table 2; Figure 2; Figure 4a). Infection rates were significantly higher in localities with high FII (Table 1; Table 2; Figure 4b). We further observed significant differences between all age categories and the highest infection rate was for 71–90 years, followed by 51–70 years and lowest in the 21–50 years (Table 1; Table 2; Figure 4c). The infection rate was higher at the stand edge than within the stand (Table 1; Table 2; Figure 4d). For higher defoliation there were higher infection rates. Only the 0–10% category did not differ significantly from the other defoliation categories, all other categories differed significantly from each other with the highest infection rate observed in the > 60–99% category, followed by the > 25–60% category and lowest in the > 10–25% category (Table 1; Table 2; Figure 4e). DBH was positively correlated with mistletoe infection (Table 1; Table 2; Figure 4f – shown as classes). Kruskal-Wallis test confirms differences between Viscum album subsp. austriacum infection rate in relation to crown part (H = 17.28, p < 0.001) with significantly higher infection rates in the upper and middle part compared to lower part (Dunn's test: middle > low, z = 2.78, p < 0.05; high > low, z = 2.41, p < 0.05) (Figure 5).
4 Discussion
Figure 5: Box plots of Viscum album infection rate (range of values 0–2) in relation to crown part (thirds). For details of display see Fig. 4. / Abbildung 5: Boxplots zum Viscum album Befall (Wertebereich 0–2) bezogen auf Kronendrittel. Für Details zur Darstellung siehe Fig. 4.
The highest Viscum album subsp. austriacum infection rate in our study was recorded in NFA Jihomoravské úvaly (South Moravia) due to high values at locality Valtice (with high FII – more drought stress). NFA 35 is located in the climatic region T4, which is the warmest in the Czech Republic. Only the edges of this NFA with higher altitude are located in the warm T2 region (Quitt 1971; ÚHÚL 1999). The average annual temperature in NFA 35 is within the range of 8.4–9.5 °C, and the average annual precipitation varies between 495 mm and 625 mm (ÚHÚL 1999). The high mistletoe infection rate in NFA 35 at locality Valtice may be attributed to its very warm and dry climate. Altitude and stand volume were the most significant predictor of the distribution of Viscum album subsp. austriacum at stand level on P. sylvestris in the Eastern Black Sea Region of Turkey (Bilgili et al. 2020b). It is commonly known that temperature decreases with higher altitude, which also applies to NFA 35 (Quitt 1971; ÚHÚL 1999). Several outbreaks of Viscum album subsp. album in NFA 35 regions have been previously reported, especially in the Lednice castle park on deciduous trees (Procházka 2004; Bulíř 2017), which is located ca 3 km from the research locality Valtice included to our study. These data indicate long-term favourable conditions for the growth of Viscum album sensu lato in NFA 35 in the warm and drought stressed areas of South Moravia.
Viscum album subsp. austriacum infection was significantly higher in trees in localities with high FII (more stressed by drought) in our study. Stands generally kept relative low or relative high FII for a long time (in comparison with other stands in the same year) (see ÚHÚL 2021). Moreover, research localities with high FII were obviously more drought stressed than the localities with low FII during our study. So, although the FII values were obtained from the Map Information Catalog for year 2017 (ÚHÚL 2021), it should not affect our study. No previous studies focused on relationship between FII and Viscum album infection are available. However, Viscum album subsp. austriacum infection lead to massive loss in photosynthetic tissue (Rigling et al. 2010) and FII depends on water content in assimilation apparatus of the stand (ÚHÚL 2021). So, massive mistletoe infection can contribute to higher FII values. On the other hand, drought is an important factor which conducive to weakening trees and making them more susceptible to the spread of biotic pests (Oliva et al., 2014), including Viscum album (Szmidla et al. 2019). Lech et al. (2020) reported a statistically significant higher Viscum album subsp. austriacum infection rate in P. sylvestris in dry sites compared to fresh, moist and very moist sites in Poland. Szmidla et al. (2019) recorded a higher occurrence of Viscum album subsp. austriacum in P. sylvestris in sites with lower precipitation in Poland. Therefore, the infection of P. sylvestris by Viscum album subsp. austriacum is higher in drier or more drought-stressed sites.
Viscum album subsp. austriacum infection was significantly higher in older trees in our study, which have larger DBH and tree height. Birds, which are the main vectors of mistletoe species, prefer taller trees for nesting and resting (Aukema and del Rio 2002). This could be one reason for more frequent infections for older and larger trees (Kołodziejek and Kołodziejek 2013; Lech et al. 2020). Our study confirms evidence in the lierature, as higher Viscum album infection rates for older P. sylvestris, Abies alba and Betula pendula trees were found in Poland (Lech et al. 2020). On Abies cephalonica, Viscum album infection was highest in trees over 100 years old in Greece (Tsopelas et al. 2004). On field maple (Acer campestre L.) and small-leaved linden (Tilia cordata Mill.) in Lednice Castle Park (South Moravia, Czech Republic), the number of Viscum album shrubs increased with tree age and lower tree vitality, with large differences between the two species (Baltazár et al. 2013). On broadleaved trees, Viscum album infection possitively correlated with tree age in the Kalingrad City (Russia) (Skrypnik et al. 2020). Thus, higher infection rate with Viscum album for older trees appears to be a general feature in Eurasian forests.
Viscum album subsp. austriacum infection was significantly higher on the trees in the stand edge than on those within the stand in our study. Kołodziejek and Kołodziejek (2013) recorded a higher Viscum album infection in stands with lower density and on the outer branches of the tree crown in P. sylvestris in Poland. Kartoolinejad et al. (2007) recorded significantly higher Viscum album infection rate in the stand edge on Parrotia persica (DC) C.A. Mey in Caspian Forests (Iran). Zuber (2004) reported that Viscum album prefers to grow in sunlit parts of the crown. Mellado and Zamora (2014) noted that excess radiation and high temperatures have a negative effect on Viscum album seeds and thus prevent its spread in warm areas on P. nigra, maritime pine (P. pinaster) and P. sylvestris in the Sierra de Baza (Spain). However, our study was performed in Central Europe, where the low temperature is a limiting factor for Viscum album (Zuber 2004). Viscum album is also a light-demanding species, especially for germination (Zuber 2004). Thus, in the climatic conditions of Central Europe, the higher occurrence of Viscum album on P. sylvestris in the stand edge can be explained by the positive effect of sunlight.
Heavily defoliated trees were the most infected by Viscum album subsp. austriacum in our study. The only exception was defoliation in the 0–10% category, due to the very low number of trees (only three). For the other defoliation categories, the numbers of trees were sufficient (115, 962, 390). Significantly higher defoliation in P. sylvestris trees infected by Viscum album was recorded also in urban area in Viernheim (Germany) (Hülsmann et al. 2013) and in forests in Teruel (Spain) (Sangüeesa-Barreda et al. 2013). Lech et al. (2020) recorded significantly higher defoliation in P. sylvestris and B. pendula trees infected by Viscum album compared with uninfected trees; in A. alba, this difference was on the border of statistical significance. The positive correlation between mistletoe infection and defoliation can be interpreted in two ways: 1) mistletoe causes higher defoliation of trees (Sangüeesa-Barreda et al. 2013); 2) heavily defoliated trees are more often infected by mistletoe, either due to the greater lightening of crowns (i.e., to favourable conditions for mistletoe growth) (Zuber 2004), or due to deteriorating health and, consequently, higher susceptibility to mistletoe attack (Dobbertin and Rigling 2006; Rigling et al. 2010). These interpretations are not mutually exclusive. Thus, the relationship between the rate of Viscum album infection and defoliation may not be unequivocally causal and consequential and is therefore a feedback relationship.
Viscum album subsp. austriacum infection increased with increasing DBH in our study, which is in line with previous studies. Sangüeesa-Barreda et al. (2013) recorded higher stem and crown diameters in P. sylvestris trees infected with Viscum album compared with uninfected ones, but trees with long-term infections of Viscum album showed reduced radial growth. Lech et al. (2020) recorded statistically significant higher DBH on trees infected with Viscum album compared with uninfected ones in P. sylvestris and A. alba; in B. pendula, the difference was on the border of statistical significance. According to the Kraft classification, predominant trees and dying or dead trees were the most infected in all three tree species (Lech et al. 2020). Significant positive correlation between Viscum album infection rate and DBH was recorded also on genera Acer, Crataegus, Junglans, Robinia and Tilia in the Lednice Castle Park (Czech Rebublic) (Baltazár et al. 2019) and on Parrotia persica in Caspian Forests (Iran) (Kartoolinejad et al. 2007). Trees with higher DBH could be more infected due to preference of bigger trees for perching it (Aukema and del Rio 2002; Kołodziejek and Kołodziejek 2013; Lech et al. 2020). Therefore, dominant trees with a higher stem diameter are more susceptible to Viscum album infection.
Viscum album subsp. austriacum infection rate in relation to crown part was lower in lower part compared to both middle and upper part in our study. This could have been caused by preference of birds for higher trees and crown sections for nesting and resting (Aukema and del Rio 2002), Moreover, Viscum album is a light-demanding species (Zuber 2004) and more light is available in upper parts of the crown compared to lower parts. Bilgili et al. (2020b) recorded gradually increasing distribution of Viscum album subsp. austriacum from lower to upper part of the crowns on P. sylvestris in Eastern Black Sea Region of Turkey, which was evaluated by the same method like in our study. Sangüeesa-Barreda et al. (2012) recorded that age and basal diameter of Viscum album subsp. austriacum increased towards the crown apex on P. sylvestris in Eastern Spain. Vallauri (1998) recorded the highest infection by Viscum album subsp. austriacum in upper third of the crown on Pinus nigra in the Saignon watershed (southwestern Alps). So, upper parts of tree crown are more susceptible to to Viscum album subsp. austriacum infection than the lower parts.
5 Conclusion
Results in our study showed that significantly higher Viscum album subsp. austriacum infection was recorded in stands with high FII (higher drought stress), in older stands (highest: 71–90 years followed by 51–70 years), on trees in the stand edge, on trees with higher DBH and higher defoliation (highest: > 60–99% then > 25–60 %, lowest: > 10–25 %), and in the upper and middle part of tree crown. These results can be explained mainly due to 1) preference of dominant trees by birds which are vectors of the mistletoe seeds, 2) lightness of the Viscum album subsp. austriacum, 3) higher susceptibity of drought stressed trees to the mistletoe infection.
In cases of continuing trends of rising temperature, more frequent drought periods and overgrowth of biotic pests, an even higher infection rate of P. sylvestris trees by Viscum album subsp. austriacum can be expected (Dobbertin et al. 2005). Therefore, planting woody varieties more resistant to drought and to high temperatures and planting in sites with lower temperatures and higher precipitations is recommended for P. sylvestris forest protection in Central Europe. The felling of infected trees leads to the lightening of stands, which may result in the further development of mistletoe on existing trees in the stand (Noetzli et al. 2003). Thus, the reduction of the rotation period can be an effective measure for P. sylvestris stand protection against Viscum album subsp. austriacum.
Acknowledgements
This study was supported by the National Agency for Agricultural Research (NAZV) of the Ministry of Agriculture of the Czech Republic, Project No. QK1920406.
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