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Article

Dispersion of Boletus-Type Spores Within and Beyond Beech Forest

by
Magdalena Wójcik-Kanach
and
Idalia Kasprzyk
*
Institute of Biology, College of Natural Sciences, University of Rzeszów, Zelwerowicza 4, 35-601 Rzeszów, Poland
*
Author to whom correspondence should be addressed.
Forests 2024, 15(12), 2232; https://doi.org/10.3390/f15122232
Submission received: 19 November 2024 / Revised: 2 December 2024 / Accepted: 17 December 2024 / Published: 19 December 2024
(This article belongs to the Section Forest Ecophysiology and Biology)
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Abstract

Basidiomycetes produce huge numbers of spores that can disperse over various distances. High spore concentrations are typically observed near the fruiting bodies, with their abundance in the air influenced by the specific habitat in which the fungi grow. The aim of this study was to investigate the concentration of airborne Boletus-type spores in a forest environment and evaluate the thesis that their dispersion beyond the forest is limited. Fungal spores were sampled in the summer and fall of 2022 in the forest, at its edge, and 1500 m away from the forest. The highest spore concentration was recorded in the forest interior, where approximately 76% of the total spores were detected. A noticeable decline in spore concentrations was observed at the forest edge, with a further significant reduction in open areas, including arable fields and mosaics of crops and heterogeneous plots, where spore presence accounted for only 12.1% of the total. During mushroom picking, airborne Boletus-type spores in the forest were unexpectedly high, so they could pose a threat to sensitized people.

1. Introduction

Basidiomycete spores are released through various mechanisms, with the most common being the ballistic discharge of ballistospores upon maturation [1]. This process relies on the formation of two distinct regions of water vapor condensation [2]. A spherical Buller’s drop is formed at the proximal end of each basidiospore (hilar appendage). At the same time, condensation occurs in a thin layer on the adaxial surface of the spore, and a second adaxial drop is formed. The drops are asymmetric in size, shape, and relative position. The Buller’s drop merges with the flattened drop on the axial side of the spore, and the result is a sudden change in the center of mass, which leads to the sudden ejection of basidiospores [3,4].
The distance of spore discharge depends on both the size of the spore and the size of the Buller’s droplets, which are dependent variables [5,6]. Experimental studies have reported varied discharge distances. Zoberi [7] experimentally showed that spores could be fired at distances from 25 µM to 300 µM, and Fischer et al. [8] reported that basidiospores are fired at different speeds, from 0.1 to 1.8 ms, and cover distances of 0.04–1.26 mm (corresponding to 9 to 63 times the length of the spores). Research conducted by Galante et al. [9] on spore deposition shows that 95% of spores fall close to the fruiting body. The dispersion scale is determined by the height of the cap, the volume of spores released, and the wind. Dan [10] questioned that experiment [9] because, according to him, the long-distance transport (LDT) factor was not taken into account. The wind spreads the spores, and their deposition is determined by gravity or washout [5]. Other studies indicate that Phlebia centrifuga spores can spread up to 1000 m [11].
Basidiomycete spores are believed to be released mainly at night, which is favored by lower temperatures and higher air humidity [12]. However, Haard and Kramer [13] presented several distinct diurnal patterns of spore release, including release around the clock as in Inocybe or Psilocybe, or the most common pattern following the daily rhythm of changes in air temperature and humidity, i.e., the maximum spore concentration in the middle of the night with a minimum during the day [1,14]. Small changes in seasonal and circadian release patterns can have significant impacts on the area where deposition occurs during the resulting dispersal event [15].
Boletes are ectomycorrhizal fungi that are symbionts of trees, such as beeches, oaks, birches, pines, firs, and spruces, and are widely distributed across temperate and subtropical regions of the Northern Hemisphere, with reports from Southern Hemisphere locations as well [16]. These fungi thrive in sunny, open forest habitats, and their fruiting bodies, valued for their culinary qualities, are collected intensively in late summer and autumn (August–October) [17]. The appearance of boletes in the forest is characterized by cyclicality, which is determined by the biology of the boletes, but also by environmental and anthropogenic factors [18,19]. The development of fruiting bodies is favored by rainfall during warm weather in summer and rainfall in autumn; poor boletes harvests are recorded during periods of drought [16]. The timing of intensive mushroom harvesting coincides with peak concentrations of basidiomycete spores in the air [17,20]. Fungal spores, including basidiomycetes, are a known source of aeroallergens [21]. This raises questions about potential health risks for sensitized individuals frequently exposed to high spore concentrations in forest environments.
The aim of this experiment was to determine the spatial differences in the concentrations of Boletus-type spores in a fresh wet upland forest and in adjacent areas outside the forest. The primary hypothesis was that maximum spore concentrations occur near the site of sporulation—within the forest—while only a small fraction of spores is detected in external environments. Additionally, this study sought to assess whether the concentrations of Boletus-type spores may pose a threat to sensitized people engaging in activities such as mushroom harvesting or exploring forest undergrowth.

2. Materials and Methods

2.1. Study Area

The research was carried out in SE Poland, in the Podkarpacie region (Figure 1), in a fresh and wet upland forest with an area of approximately 1300 ha (49°57′ N, 21°47′ E) [22]. The forest is diverse in terms of phytosociology, as there are mixed and deciduous forests. The forest stands, depending on the community, are dominated by Fagus silvatica, Picea excelsa, Quercus robur, and Pinus silvestris [22]. Its most valuable natural part is the Wielki Las nature reserve, which protects Carpathian beech forest with old beech trees. In addition to Fagus silvatica, there are numerous Abies alba and Acer pseudoplanatnus trees. The herbaceous vegetation consists of mountain and submountain species, such as Polystichum aculeatum, Allium ursinum, Veronica montana, Sambucus racemosa, Aposeris foetida, Dryopteris dilatate, Chaerophyllum hirsutum, and Equisetum telmateia. The most valuable species include orchids—Cephalanthera longifolia and Neottia nidus-avis.

2.2. Aerobiological Monitoring

The aerobiological experiment was conducted from early July to late November 2022, a period characterized by favorable conditions for the development of boletes [23]. Two types of volumetric traps were used: portable and stationary, for short-term and continuous monitoring, respectively.
Air sampling was carried out by portable traps at 4 sites. Two sites (ST 1 and ST 2) were located within the forest, while a third site (ST 3) was located at its edge. The sites were located in a straight line approximately 250 m apart. The fourth site (ST 4) was located outside the forest, approximately 1500 m from its edge. This distance was selected as it exceeds the influence of forest microhabitats, which extends up to 50 m beyond the forest edge [24]. A Burkard portable sampler sucked 10 L of air per minute directly onto a microscopic slide covered with silicon as a sticky medium. During this experiment, the trap worked for 10 min at each site, so the measurement campaign on one day at all sites lasted one hour. Samplings were carried out every second/third day before noon. Furthermore, during air sampling, meteorological parameters were monitored, that is, air temperature, humidity, wind speed, and pressure, using a portable Kestrel 5500 gauge.
At ST 4, continuous monitoring was conducted using a 7-day Lanzoni trap, a device based on the Hirst-type sampler (Figure 1). It also sucked 10 L of air per minute, and the spores were covered with sticky silicone Melinex tape placed inside the device. Once a week, this transparent tape was removed and microscopic slides were prepared in the laboratory. The results obtained using this method were considered as a reference. Furthermore, at this station, meteorological parameters were monitored, i.e., minimum temperature, maximum temperature, average temperature, precipitation, humidity, and wind speed (Davis Vantage Pro2 stationary meteorological station).
Boletus-type spores were identified and counted using a light microscope at 600× magnification. For short-term monitoring with the portable sampler, spores were analyzed over the entire sampling area of 52.0 mm2 on the microscope slide. For continuous monitoring with the Lanzoni trap, spores were analyzed along a single horizontal strip of 16.8 mm2 on the tape. The results were calculated and given as the number of spores in 1 m3 of air and the average daily concentration of spores in 1 m3 of air, respectively, depending on the method used. The literature states that the Boletus type is mainly represented by spores of fungi from the genus Boletus, Chroogomphus, Gomphidius, Leccinum, Suillus, and Xerocomus [25]; therefore, in this article, the authors adopted the classification of Boletus type.

2.3. Data Analysis

The basic characteristics of the season of occurrence of spores in the air were presented, i.e., the day of the maximum concentration of spores in the air and the maximum concentration of spores at each site. For the results obtained using a 7-day Lanzoni trap (Hirst trap), the following statistics were calculated: the length of the season, determined by the 90% method; its beginning and end; its intensity, expressed as Seasonal Spore Integral (SSIn); and the number of days (frequency-f) in which at least one spore was found in the air. For the data obtained by the Burkard portable trap, the total number of spores determined during the experiment was given. The synchronization of the periods of spore occurrence in the air at the ST 1–ST 4 was examined using Spearman rank correlation by calculating the correlation coefficient (rs).
The dispersion of spores from the forest was analyzed by comparing the average spore concentrations at each site. The forest (ST 1) was considered to be the main source of spores, and the number of spores detected there was considered to be 100%. The concentrations at ST 3 (forest edge) and ST 4 (open area) were expressed as percentages relative to this baseline. The differences in spore concentrations between ST 1 and ST 3 as well as between ST 1 and ST 4 reflect the percentage of trapped forest spores. These sites were also compared in terms of spore concentrations in the air using the nonparametric Kruskal–Wallis test, followed by post hoc multiple comparisons with Dunn’s test, because the data did not conform to a normal distribution. A significance level of α ≤ 0.05 was applied for all tests. All statistical analyses were performed using Statistica version 13 software.

3. Results

3.1. Comparison of Meteorological Conditions at ST1–ST4

The air temperature recorded at the time of aeromycological sampling decreased as one approached its edge. The average air humidity was the lowest at ST 4. Slightly higher air humidity was recorded in the forest (ST 1–ST 3), ranging from 72 to 74%. The air pressure was the highest outside the forest (ST 4) and the lowest in the forest (ST 1). The temperature of the dew point, determined based on the values of the parameters described above, was lower at the ST 4 by 1.2 degrees compared to the forest site (ST 1) (Table 1).

3.2. Short-Term Aerobiological Monitoring

The analysis showed that the sites differed significantly in terms of the spores recorded in the air (H = 7.876; p = 0.048). The statistically significant difference relates to the site located in the forest (ST1) and the site furthest from it (ST4). The latter was characterized by the lowest spores, the lowest maximum value, and the lowest variability in the results (Figure 2).
A total of more than 31,000 spores were found at the site located in the forest interior (ST 1) (Table 2). In August and September, spore concentrations generally did not exceed 1000 spores in m3 of the air. High spore concentrations were recorded in the first two decades of October, with maximum concentrations on October 13 (Figure 3). At the second site located in the forest (ST 2), almost 29,000 spores were determined and almost half of them were detected in one day, that is, on October 11. This was the highest value found during the investigation (Table 2). Unlike the other sites, no increased concentrations of spores in the air were found at the end of August (Figure 2). At the site located on the edge of the forest (ST 3), more than four times fewer spores were recorded than in the forest interior (ST 1) (Table 2). In the last days of August, the spore concentration was low, ranging from 130 to 220 spores in m3 of the air. A clear increase in concentrations was observed on October 8. The maximum concentration was recorded on the same day as at ST 2, although its value was more than seven times lower (Figure 3). At the site located outside of the forest (ST 4), the sum and maximum values of the total spores were the lowest among all sites studied (Table 2). In August and September, bolete spore concentrations were not high; the sudden increase in concentration and the maximum concentration were recorded on the same days as at ST 3, October 8 and 11, respectively (Figure 3).
The courses of spore occurrence in the air at sites located in the forest (ST 1, ST 2) and at the edge of the forest (ST 3) were quite similar. The pattern of spore occurrence outside the forest was slightly different; the spores remained in the air longer in significant numbers and the synchronization in relation to ST 1, ST 2, and ST 3 was rs = 0.483, rs = 0.663, and rs = 0.645, respectively.
It was assumed that the main source of Boletus-type spores was the forest, and the number of spores detected at ST 1 was 100%. A clear decrease in the spore concentration was visible at the edge of the forest, and at ST 3 the percentage share of spores was 24.1%. In turn, in open parts of arable areas and complex systems of crops and plots (ST 4), approximately 1500 m from the forest, the number of spores was low and constituted 12.1% of the sum recorded at ST 1. It can be concluded that approximately 76% of Boletus-type spores produced in the forest are not dispersed outside it (Figure 4).

3.3. Continuous Aerobiological Monitoring

Continuous air monitoring was also carried out, and the obtained results constituted a reference. It was found that from the beginning of July to the end of November, the frequency of days on which at least one Boletus-type spore was found in the air was over 80% (Table 2). From the beginning of July to the end of November, the daily concentration of spores in the air fluctuated, and three periods with an increase in spore concentration in the air were observed. The first was observed in July, and the average daily spore concentration on those days did not exceed 90 spores in m3 of the air. The next increase in spore concentration lasted for almost all of August, with the highest concentrations in the third part of that month. The last increase in spore concentration was recorded in October. This was the time when average daily spore concentrations were the highest throughout the season, often over 200 spores per m3 of air (Figure 5). On 17 October, the maximum spore concentration in the season was recorded, that is, 1668 spores in m3 of the air (Table 2). The use of continuous monitoring allowed for tracking of the daily cycle. The lowest concentrations were found between 9 a.m. and 2 p.m. and the highest between the afternoon and night hours, that is, between 5 p.m. and 11 p.m. (Figure 6).
It is worth noting that on October 13, when a high concentration was recorded in the morning on ST 1, at the same time, the number of spores recorded outside the forest using the continuous monitoring method was very low or no spores were recorded at all. Their maximum concentrations were recorded much later, i.e., at 4 p.m. and 9 p.m. A similar phenomenon was observed on October 16.

4. Discussion

Seasonal spore concentrations are characterized by marked variability [21,26]. In warm climates, bolete spores can be present in the air for nearly the entire year. In Turkey and Spain, studies revealed an absence of spores during early spring (March and April), with concentrations beginning to increase in May; in both countries, the period with high concentrations occurred twice a year, but in different months [25,27]. In Turkey, the period with the highest concentrations was recorded mainly in autumn, with spores remaining abundant even during winter (December and January) [27]. Conversely, in Spain, high concentrations already appeared in June and then in late autumn in November [25]. Furthermore, Grinn-Gofroń et al. [28] proved that within the Black Sea Basin in Turkey, the timing of maximum concentrations of Boletus-type spores can vary by more than 130 days. In Poland, in warm temperate climates, single spores usually appear in spring, with continuous presence in the air starting in June. Peak concentrations, however, occur in late summer and autumn [21].
The season of the occurrence of Boletus-type spores in the air and its intensity often correspond with the mushroom picking season in forests. In Poland, the 2022 mushroom harvest was slightly above average, but started slightly later than usual, from the end of September to mid-October. In the Podkarpacie region, in the area where this research was carried out, the first mushrooms appeared at the beginning of August [29], coinciding with a significant increase in spore concentrations, as confirmed by aerobiological monitoring. The main mushroom picking period began at the end of September [29]. During this time, the number of people visiting the forest and exploiting the forest undergrowth was the highest (own observations).
In general, mushrooms are believed not to be a significant cause of inhalant allergies, and reports on this topic are not frequent. Boletes are particularly eagerly collected by mushroom pickers, and there are reports of their allergenic effects, but not due to spores [30,31,32]. The possibility of hypersensitivity to Boletus spore allergens was confirmed by Lehrer et al. [33]. Clinical studies by Helbling et al. [34] and Lehrer et al. [33] found that 5% to 10% of tested patients reacted to Boletus spore allergen extracts. Forest environments are often perceived as clean and free from pollution, which attracts individuals seeking outdoor recreation. Since we have shown that during mass mushroom occurrence [17], the concentrations of spores in the forest were unexpectedly high, and they could theoretically pose a threat to sensitized people. A potentially dangerous situation is the collection of mushrooms. People lean over them and cause mechanical vibrations of the mushroom’s fruiting body, releasing a mass of spores from the cap. During this research, record concentrations of spores in the forest (ST 1 and ST 2) exceeded 9.5 thousand and 16 thousand in 1 m3 of air, respectively. Considering that an adult inhales approximately 0.5 to 0.6 L of air per breath, mushroom collectors could inhale several Boletus-type spores with each breath. Certainly, allergenic spores of other basidiogenic fungi (e.g., Coprinus) or mitosporic fungi (such as Alternaria, Epicoccum, or Cladosporium) are also inhaled [34,35,36,37]. So, it can be concluded that airborne spores could be a potential disadvantage in forest ecosystems.
The main source of airborne basidiospores, such as Boletus, is the forest [11], which was confirmed by our research. The literature on this subject shows that the spores of mushrooms are launched over short distances, and the wind is the main vector of their dispersion [5,8,9,15,38]. The anemometric conditions of the forest are crucial. The wind quickly loses strength as it enters the forest. When there is a strong wind, its speed decreases in the crowns and increases in the trunk zone [39], although these differ in the case of coniferous and deciduous trees [40]. Even on windless days in the forest, you can observe air movements due to differences in humidity and thermal conditions. As a result of uneven heating of the forest (e.g., ST 1 and ST 2 located in horizontal profile 250 m apart), an air pressure difference arises and vertical, horizontal, and turbulent air flows are created, which favor the dispersion of sporomorphs, including fungal spores [39,41,42]. The flight time of the spores depends mainly on turbulence, i.e., convection during the day and weaker turbulence at night. Mushrooms actively discharge spores at low altitudes [12]; however, they can then control to some extent the further dispersal of the spores, which was previously considered a passive phase [15,38]. Evaporating water from the cap cools the surrounding air, which causes slow air movements that carry spores from under the mushroom cap, and convective air flows are created that transport spores several dozen centimeters upward, which was proven experimentally [43]. Due to such mechanisms, cap spores can escape from the forest. The forest edge zone presents a noticeable change in microenvironmental conditions, including light intensity, humidity, water vapor pressure, and temperature ([24], Table 1). This transition zone is associated with a marked drop in spore concentrations (ST 3). It is also noteworthy that spores remained airborne for a longer period at the site located outside the forest (ST 4) compared to its center (ST 1). This observation suggests that, in addition to the forest, other areas also contribute to spore presence, indicating medium- or long-distance transport [38], and further supporting the hypothesis of regional spore influx.

5. Conclusions

To properly understand the process of the dispersal of Boletus-type spores, it is crucial not only to know the biology of these fungi, including seasonal and circadian variability, but also to be able to analyze the abiotic processes of the environment in which they occur. Forest ecosystems serve as the primary habitat for fungal spores and can act as both a source and a barrier to their dispersion. The concentration of Boletus-type spores is the highest within the forest, with a marked decrease observed at the forest edges. However, phenomena that favor the transport of spores to other, nonforest microhabitats cannot be ruled out. The mechanism of spore transport and their distribution may have significant implications for human health. Our findings suggest that the forest may pose a threat to individuals with allergies to airborne fungal spores. Consequently, forest walks should take place during periods of low spore concentrations to mitigate potential health risks.

Author Contributions

Conceptualization, I.K. and M.W.-K.; Methodology, I.K. and M.W.-K.; Software, M.W.-K.; Validation, M.W.-K. and I.K.; Formal Analysis, M.W.-K.; Investigation, M.W.-K.; Resources, M.W.-K.; Data Curation, I.K.; Writing—Original Draft Preparation, M.W.-K. and I.K.; Writing—Review and Editing, M.W.-K. and I.K.; Visualization, M.W.-K.; Supervision, I.K.; Project Administration, I.K.; Funding Acquisition, I.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data presented in this study are available on reasonable request from the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Location of research stations (ST 1–ST 4) against the background of vegetation cover type.
Figure 1. Location of research stations (ST 1–ST 4) against the background of vegetation cover type.
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Figure 2. Homogeneous groups of sites (same letters) distinguished based on the comparison of spore concentrations using the Kruskal–Wallis test with multiple comparisons using Dunn’s test.
Figure 2. Homogeneous groups of sites (same letters) distinguished based on the comparison of spore concentrations using the Kruskal–Wallis test with multiple comparisons using Dunn’s test.
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Figure 3. Concentrations of Boletus-type spores at research sites (ST 1–ST 4) in August–November 2022.
Figure 3. Concentrations of Boletus-type spores at research sites (ST 1–ST 4) in August–November 2022.
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Figure 4. Dispersal of Boletus-type spores inside and outside forest.
Figure 4. Dispersal of Boletus-type spores inside and outside forest.
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Figure 5. Boletus-type spore concentrations detected by stationary trap.
Figure 5. Boletus-type spore concentrations detected by stationary trap.
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Figure 6. The hourly concentrations (UTC+02:00) of airborne Boletus-type spores (spores in m3).
Figure 6. The hourly concentrations (UTC+02:00) of airborne Boletus-type spores (spores in m3).
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Table 1. Average values of meteorological parameters during the period of aeromycological research.
Table 1. Average values of meteorological parameters during the period of aeromycological research.
StationTmean
(°C)		Humidity
(%)		Pressure
(hPa)		Dew Point
(°C)		Wind Speed
(m/s)
ST 114.772.1980.29.50.5
ST 214.172.5981.78.70.9
ST 313.874.3982.48.90.6
ST 414.070.4993.78.30.6
Table 2. Characteristics of Boletus-type spore season at research stations (ST 1–ST 4) and at 24 h air monitoring station in 2022. f—frequency.
Table 2. Characteristics of Boletus-type spore season at research stations (ST 1–ST 4) and at 24 h air monitoring station in 2022. f—frequency.
Short-Term Monitoring—Burkard Portable Sampler
stationtotal sum
of spores		max concentration
(spores in m3 of the air)		day of
max concentration
ST 131,050955013 October
ST 228,79016,16011 October
ST 37470216011 October
ST 4377082011 October
Continuous monitoring—Lanzoni trap
length
of season (days)		SSInstart of season (day)end of season
(day)		f
(%)		max concentration
(spores in m3/24 h)		day of
max concentration
7113,81416 August25 October82.4116817 October
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Wójcik-Kanach, M.; Kasprzyk, I. Dispersion of Boletus-Type Spores Within and Beyond Beech Forest. Forests 2024, 15, 2232. https://doi.org/10.3390/f15122232

AMA Style

Wójcik-Kanach M, Kasprzyk I. Dispersion of Boletus-Type Spores Within and Beyond Beech Forest. Forests. 2024; 15(12):2232. https://doi.org/10.3390/f15122232

Chicago/Turabian Style

Wójcik-Kanach, Magdalena, and Idalia Kasprzyk. 2024. "Dispersion of Boletus-Type Spores Within and Beyond Beech Forest" Forests 15, no. 12: 2232. https://doi.org/10.3390/f15122232

APA Style

Wójcik-Kanach, M., & Kasprzyk, I. (2024). Dispersion of Boletus-Type Spores Within and Beyond Beech Forest. Forests, 15(12), 2232. https://doi.org/10.3390/f15122232

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