Review of the most important fungal diseases occurring in forest nurseries in Poland in 2012–2021

Over a period of ten years, data was systematically collected on the occurrence of pathogens in forest nurseries. Several categories of diseases of planting material were recorded as part of the study, including diseases such as oak powdery mildew (Erysiphe alphitoides (Griffon & Maubl.) U. Braun & S. Takam.), dampingoff (Fusarium spp, Cylindrocarpon spp., Rhizoctonia solani, Phytophthora spp., Pythium spp.), needle-cast of pine (mainly Lophodermium seditiosum Minter, Staley & Millar), pine twisting rust (Melampsora pinitorqua (Pers.) P. Karst.) and gray mold (Botrytis cinerea Pers.). The areas in which all diseases have occurred in the last ten years are summarized in the chart (Fig. 1).

Figure 1.

Area of occurrence of the most important fungal diseases in nurseries in Poland in the period 2012–2021

It should be noted that not only the areas of pathogen occurrence but also the production areas of the forest nurseries changed during the period analysed. The collected data show that in 2012 the production area of the forest nurseries managed by the State Forests was 2281.89 ha and 848,527.85 thousand trees and shrubs were produced there annually. Since then, there has been a downward trend and each year the production area has decreased, resulting in fewer plants being produced (Tab. 1).

Among the diseases mentioned above, the greatest area of damage was recorded for oak powdery mildew (Erysiphe alphitoides). Powdery mildew is a large group of fungi with specialised pathogens for most plant species except conifers (Jakuschkin et al. 2016). It appears as a dusty, white, or grey coating on the surface of leaves or other plant parts. These diseases are caused by a group of fungi from the ascomycete family (Erysiphaceae) that grow superficially on the leaves, and only haustoria penetrate the cells. Conidia form in large numbers in the form of powdery masses on the infected leaves. The teleomorph of the fungi from the Erysiphaceae family is cleistothecia, which develops between the mycelium and are visible to the naked eye as black dots when mature. Powdery mildew fungal pathogens infect the aerial parts of higher plants and rarely kill their hosts, but their pathogenesis results in significant yield losses mainly due to the removal of nutrients from the host plant, reduction in photosynthesis, stunted growth and increased respiration and transpiration (Wu et al. 2021). A more common consequence of powdery mildew infection is reduced carbon uptake. As biotrophic parasites, powdery mildew fungi obtain their nutrients from living host cells thanks to specialised nutritional structures called haustoria (Divon and Fluhr 2007). Powdery mildew infection can lead to the distortion of young growing leaves (Takamatsu et al. 2007; Hajji et al. 2009; Jakuschkin et al. 2016).

Oak powdery mildew occupies a special place among the biotic factors that threaten English oaks and their regeneration. It is known from the literature that climatic conditions have a significant influence on the development of this organism. For instance, Hewitt’s (1974) investigations explored the interplay between temperature and relative humidity on the growth rate of powdery mildew, revealing that an optimal temperature of 25°C and 96% relative humidity promoted the swiftest growth. Additionally, conidia was observed to expand at relatively low humidity levels of just 32%. It is worth noting that the temperature range of 15–25°C was discovered to be most conducive to the growth of powdery mildew. There are many reports showing the relationship between temperature and the germination rate of powdery mildew conidia. According to Škorić (1926), optimal fungal growth requires a temperature of 26–28°C. However, Karadžić and Milijašević (2005), reported that the conidia of oak powdery mildew germinated most intensively in the range of 20–30°C and a relative humidity of 76–96%. Relative humidity is not a limiting factor for the germination of conidia, especially in the early stages of germination. In contrast, other studies have demonstrated that increased humidity is advantageous and even necessary for the development and spread of oak powdery mildew (Pap et al. 2013). Many authors emphasise the detrimental effects of saturated humidity on powdery mildew conidia germination (Nour 1958; Zaracovitis 1966; Uchiyama et al. 1978; Yarwood 1978; Mishina and Talieva 1987; Chellemi and Marois 1991). The last important factor mentioned in the literature for the development of this disease is the influence of light on the development of oak powdery mildew. It is known from many reports that light stimulates the formation and spread of epiphytic mycelium on leaves (Kelly 2002; Giertych and Suszka 2010). It is known that plants exposed to intense light are highly susceptible to parasitic fungi from the order Erysiphales. This phenomenon can be explained by the fact that they are obligate parasites that require organic substances from living cells for their development, which are abundant in plants with intensive assimilation through strong light (Pap et al. 2013).

By Polish standards, a decline in the number of damaged areas caused by oak powdery mildew was observed during the period analysed (Fig. 2). The greatest intensity of this disease was recorded in 2013, when it occurred on an area of 245 ha. From the maps attached below, it can be concluded that the greatest intensity was recorded in the eastern part of the country. In the following years, a systematic decrease in the severity of the disease was observed, and in 2021 it occurred only on 118 ha.

Figure 2.

Location of Powdery Mildew occurrence in the years 2012–2021, divided by Regional Directorates of the State Forests

The pathogenic seedling blight in the years 2012–2021 it remained at a similar level (Fig. 1). Damping-of is a disease of young plants that leads to death within a few weeks of germination. A large group of fungi (belonging to the genera Cylindrocarpon, Fusarium, and Rhizoctonia) and oomycetes (Phytophthora and Pythium) are responsible for this phenomenon (Mittal and Wang 1993; Sutherland et al. 2002; Darvas et al. 1978; Lilja et al. 2010; Lamichhane et al. 2017; Asaka and Shoda 1996; Jung et al. 2016). The total area of damage caused by pathogenic damping-off was almost 1350 ha during the years 2012–2021. It is the second most common disease entity in Poland. For this assessment, pathogenic damping-off on coniferous and deciduous seedlings were considered separately. The first group was more numerous. Damping-off of conifer seedlings in Polish nurseries was mainly infections of Scots pine. In the last ten years, it has remained relatively constant at around 100 ha per year. Major damages were recorded in 2012 (111 ha), 2013 (92 ha), and 2019 (85 ha). The second group was the damping-off of deciduous tree seedlings. This disease mainly affected oaks and beeches, however, alder and birch dieback have also been reported. From 2012 to 2021, a systematic decrease in damage caused by the damping-off of deciduous tree seedlings was observed. A sudden change was observed in 2020, when the area of damage was recorded at 65 ha, while the average value over the entire 10-year period was 54 ha. For this disease as a whole (conifers and deciduous trees), it is difficult to speak of a trend in terms of the intensity of the disease in certain parts of the country, especially in the first years of observation (Fig. 3).

Figure 3.

Location of Damping-off occurrence in the years 2012-2021, divided by Regional Directorates of the State Forests

The next disease that has become widespread in the last ten years has been needle-cast of pine. This is a disease that affects conifers. The first symptoms of the disease can appear on pine trees in September and October as small yellow or brown spots on needles (Diwani and Millar 1987). Infected needles turn brown and fall off the tree the following spring (Martinsson 1975; Kurkela 1979). Lophodermium is a genus of ascospores fungi that contains both needle pathogens and endophytes of conifer hosts (Müller and Hallaksela 1998). Although Minter et al. (1978) recognised at least four species of Lophodermium that can infect pine needles, only L. seditiosum is considered pathogenic (Diwani and Millar 1987: Kurkela 1979). Ascocarps of L. seditiosum mature on fallen needles (Diwani and Millar 1990) and begin to release ascospores in late summer, with the peak of their development in Europe occurring in September and October (Diwani and Millar 1990). High rainfall in late summer and autumn creates favourable conditions for infection (Lilja et al. 2010; Diwani and Millar 1990). Climatic factors, such as lower autumn temperatures and early snow cover, could explain the lower risk of disease (Lilja et al. 2010). Nevertheless, the maximum development of the disease can occur in early summer. This fact is attributed to favourable temperatures combined with higher relative humidity and frequent rainfall, that coincide with the formation of the first pine needles. Warm, humid summers and the abundance of young, susceptible hosts favor the development of the disease (Woods 2003; Aminev 1980; Kowalski 1982; Hanso and Hanso 2001). Drenkhan (2010) found that occurrence of the needle-cast of pine in Switzerland was related to higher precipitation and higher humidity in summer, while Wyka et al. (2017) found that warmer climates and wetter springs favored the development of needle diseases in white pine (P. strobus L.), but they found a lower probability of disease occurrence with higher winter precipitation and higher humidity. Pagony and Gasko (1977) also observed disease epidemics caused by the high density and humidity of seedlings, which in the context of nursery production is a very important factor influencing the damage caused by this pathogen. In the study by Pandit et al. (2020), which used the MaxEnt SDM climate model, it was again shown that in the area they analysed (southeastern USA), the occurrence of the needle-casts was related to the average dew point, vapour pressure deficit and precipitation in the cold season. The climatic factors they identified as important for the occurrence of the disease – precipitation and hu midity – were consistent with other studies (Boyce 1969; Drenkhan 2010; Wyka et al. 2017).

The occurrence of pine needle-casts is the third most common disease in Polish forest nurseries. In 2012, damage caused by this disease was recorded on a total area of 111 ha. The largest areas of damage are observed in the north-western part of Poland (Fig. 4). As with most of the diseases discussed, a downward trend in the area of damage is observed from year to year. In 2021, the pine disease was detected on 66 ha, which corresponds to a decrease of almost 50% within a decade.

Figure 4.

Location of Needle-cast of pine occurrence in the years 2012–2021, divided by Regional Directorates of the State Forests

Early symptoms of gray mold can be recognised by a greyish, cotton-like mycelium and spores on tree-like conidiophores. The pathogen Botryotinia fuckeliana (de Bary) Whetzel is a saprophytic ascomycete whose asexual stage (Botrytis cinerea) is frequently found in forest nurseries (Gregory and Redfern 1987; Peterson et al. 1988; Sutherland and Davis 1991). Infection with B. cinerea often occurs following abiotic damage, such as frost, fertiliser, or herbicide application (Sutherland and Davis 1991), although low light intensity combined with environmental stress (e.g. 30–40°C or prolonged drought) may also be important as predisposing factors (Zhang and Sutton 1994; Zhang et al. 1995). Gray mold spores are transmitted by humans, flying insects (James et al. 1995), wind and greenhouse ventilation (Sutherland and Davis 1991). The spores germinate at temperatures from 0 to 25°C, whereby the germination rate depends on the temperature and is optimal at 7–20°C (Petäistö 2006). Russell (1990) found that infection can occur after only three hours at 15–20°C and 98% relative humidity if there is free water on the plant surface. Although gray mold infection was thought to start on the lowest, weakened or dead parts of the seedlings before penetrating healthy tissue (Sutherland and Davis 1991), infection of spruce was found to be more severe in the upper parts of the seedlings at 6°C and 80–90% relative humidity (Petäistö 2006).

In Polish nurseries, this disease occurred on average in an area of approximately 13.5 ha from 2012 to 2021. Throughout the analysed period, the area of damage caused by B. cinerea fungus fluctuated slightly, with the lowest value in 2019 (9 ha in the whole of Poland) and the highest in 2012 (20 ha). When looking at the map showing the damage caused by gray mold in Poland, it is difficult to identify a trend in terms of distribution (Fig. 5).

Figure 5.

Location of Gray Mold occurrence in the period 2012–2021, divided by Regional Directorates of the State Forests

Pine twisted rust is caused by Melampsora pinitorqua. This disease occurs sporadically in nurseries and poses a significant threat to pine stands (Jalkanen and Kurkela 1984). An alternative host for this pathogen is often aspen poplar (Populus tremula L.), where the rust overwinters in the form of teliospores on fallen aspen leaves. Under natural conditions, the teliospores germinate in spring after rainfall and produce basidiospores that infect the leading shoots of pine in the current year. Kurkela (1973a, b) studied the dispersal of basidiospores in June in three consecutive years and found that basidi ospores were formed and released at temperatures between 0 and 27°C (with a maximum of 15–20°C), with maximum spore number and density varying considerably from year to year. Rain plays a crucial role in the formation and release of basidiospores, and it also affects the degree of infection (Klingström 1963; Kurkela 1973a).

Similar to the previously described gray mold, pine twisting rust is not a major problem in Polish forest nurseries, but every year a small area of damage causing from this disease is reported. The damages caused by M. pinitorqua averaged 19.7 ha during the analysed period. As with most pathogens analysed, the largest area of damage was recorded in 2012 (almost 30 ha across the country), and since then there has been a gradual decline to 15.7 ha in 2020. Every year, a significant area of damage caused by pine twisting rust is reported mainly in the eastern part of Poland (Fig. 6).

Figure 6.

Location of Pine Twisting Rust occurrence in the period 2012–2021, divided by Regional Directorates of the State Forests

Finally, it is important to consider abiotic factors, which can also capable of seriously damaging forest nurseries. However, the data collected between 2012 and 2021 did not record any instances of this phenomenon. It is important to note that the absence of recorded instances does not necessarily mean that this problem does not occur. The factors that cause abiotic diseases in seedlings are primarily unfavourable weather conditions for their development: temperature drops, prolonged drought with high temperatures, sudden and/or prolonged rainfall and hailstorms. The most frequently observed problems in forest nurseries are certainly sunburn, flooding of the roots with water, mechanical damage or frost, which can manifest itself in characteristic discolouration of the assimilation apparatus (e.g. needles).