Influence of Environmental Factors on the Concentration of Fungal Spores in the Air

1. Introduction

It is well known that indoor aerosols can contain a wide variety of pathogenic and allergenic fungi [1,2]. These include representatives of the genera Alternaria, Aspergillus, Cladosporium, and Penicillium. These fungi enter indoor air from both indoor aerosol sources and the atmosphere.

Atmospheric aerosols contain a wide variety of culturable microorganisms, including representatives of fungi of all groups living in soil, plants, animals, aquatic and other systems of the Earth [3,4,5,6,7]. Propagules of microscopic fungi (conidia, spores, mycelium) enter the air from the soil with dust particles, from plants, fruits and animals; they are carried with air currents over long distances, including transcontinental ones, and colonize new suitable substrates [8,9,10,11]. As a result, fungi are found in wildlife, participate in a variety of processes, and often play a positive role in the maintenance and functioning of any natural ecosystem. Fungi also play a negative role, causing various diseases in humans, animals, and cultivated plants, as well as damage to materials, including food products, industrial structures, archival documents, and art’s masterpieces. Researchers are interested in aerobiological studies that consider the quantitative and taxonomic composition of fungal spores in the air for several reasons [12]:

1) fungal spores play an important role as a trigger for the development of allergic diseases in humans;

2) The study of “fungi’s aerosol” allows us to determine the degree of resilience of ecosystems in connection with global warming;

3) geospatial distribution of fungal spores, as one of the main components of bioaerosols, and their transport over long distances.

The main source of fungal spores in the air is surface mycobiota (molds, plant parasites and other fungi living on plants, on the soil surface, on man-made substrates, in the surface monolayer of water bodies, etc.) [3,13,14,15,16]. Most species of fungi have special mechanisms by which they can actively release spores into a freely moving turbulent layer of air [13,17,18,19,20,21]. But even without active release of spores, constant wind erosion causes them to be blown away from plants, with soil particles and water splashes, enter the atmosphere again, increasing the concentration of aerosol in the air.

Knowledge of the diversity of fungi in the air and the impact of various meteorological factors on their concentrations in the atmosphere is of great importance for solving a number of fundamental and applied issues related to medicine, agriculture, and ecology. There are quite a lot of publications in the literature about the presence of fungi in indoor air and their impact on human health, but they will remain outside the scope of this review. The aim of the work is to review the information presented in the literature concerning only fungi in atmospheric aerosol and the influence of environmental factors on them.

2. The Influence of Environmental Factors on the Concentration of Fungal Spores in the Atmosphere

The concentration of fungal spores in the atmosphere is the result of complex interactions between biotic and abiotic environmental factors, which include geographic location, weather conditions, time of day, air pollution, the presence of vegetation, animals, humans, etc. The total number of spores in the aerosol varies from a few species to 4×10⁵ m^-3 [4,5,6,22,23,24,25,26,27,28,29]. Some spores are characterized by a pronounced circadian (daily) periodicity of appearance in the bioaerosol, although for other fungi this may not be observed [30,31,32,33].

In some regions, fungal spores make the largest contribution to the composition of bioaerosols. For example, according to publications [34,35,36,37], this is the case, in particular, in the Amazon River basin. Modeling by Heald and Spracklen [38] led to the conclusion that 23% of all primary organic aerosol emissions are due to fungi. Similar calculations [25,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81] were later extended to include fungi acting as ice nuclei in clouds in [39]. In general, fungi in atmospheric aerosols predominate in the air of some regions [31,32,33,34,35,36,37,38,39,40,41,42], while in other regions bacterial aerosols predominate [42,43,44,45,46].

Currently, research is actively underway in different countries of the world, on different continents, to study the effect of meteorological factors on the concentration of spores [25,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81]. The results of numerous studies using multiple regression analysis show the absence of a unified model of the influence of meteorological variables on the number of spores and their qualitative composition. Various combinations of factors determine the concentration of spores of different types of fungi. The individual value of each parameter is difficult to estimate due to the dynamic nature of the atmosphere [32,55,63,68,72,82]. However, temperature and dew point (or the relative humidity associated with it) are considered by many researchers to be the most important [83,84,85,86,87]. Significant correlations have been established for different geographical regions between the number of spores of individual fungal species, temperature, and relative humidity [53,57,59,60,62,67,75,78,81,84,896]. It was revealed that during the day, changes in the concentration of spores of individual fungal genera had three variants: in the morning, the maximum values were reached by Cladosporium spores, nighttime peaks were for Coprinus and Leptosphaeria, and simultaneously, different behavior throughout the day was noted for Aspergillus/Penicillium spores [22,31,93,97]. The influence of extreme weather events on the concentration of spores in the air should also be mentioned [98,99].

The average air temperature significantly affects not only the abundance of micromycetes in the air, but also accelerates the onset of spore seasons. The early start and late end of the season determines its extension from 20 to 60 days, depending on the geographical location. The time to reach the cumulative amount of 50% of the spores can be reduced to 25 days. For Cladosporium, the acceleration of the moment of maximum spore concentration per m³ of air was found to be from 26 to 56 days [63,82,100]. The spores of moisture-loving fungi (Didymella, Ganoderma) are more sensitive to weather changes, in contrast to dry-spore species (Alternaria, Botrytis, Cladosporium) [61,100,101,102,103]. Long-term studies of the concentration of Alternaria and Cladosporium spores in the atmosphere of seven countries and four biogeographic regions of Europe have shown that local climate, vegetation and landscape management structure are the determining parameters for the total concentration of spores. The air temperature and wind speed determine the season of the spores of these species [28,48,59,67,92,98,101,104,105,106,107,108,109,110]. In [30], the maximum wind speed and minimum relative humidity are indicated as the most effective independent variables for predicting the general trend in the concentration of Alternaria spores in the air. Weekly concentrations of Alternaria spores in the atmosphere can be predicted based on the expected maximum temperature and concentration of spores during the year. The values of the concentration of Cladosporium spores per week can be predicted based on the concentration of spores of fungi of the genus Alternaria [107[. A prognostic model has also been developed for fungi of the genus Ganoderma [111].

Attempts have been made to build monthly models for predicting the concentration of Alternaria spores in the air based on data on humidity, as the most important variable, on the day of the study. This is a new approach to modeling time series with short spore seasons, which makes it possible to predict the concentration of Alternaria spores with high accuracy [59,112]. A model for the prediction of fungi aerosol concentration dynamics in the surface layer of the atmosphere was developed in Russia [113] and a model based on the analysis of fungal DNA in the air was described in [114].

A study of the duration of the Alternaria spore season in central and eastern Europe showed that, regardless of geographical location, the first stage (0-0.9% of Alternaria spores in the air) was the longest (up to 60 days), and the last (97.5 to 99% of fungal spores) was the shortest (22 days or less). There was a significant variation in the number of spores per cubic meter of air (from 139 in the north to 2295 in the central part of Europe). The number of days exceeding the threshold value of 300 spores per m³, associated with serious health problems in atopic people, varied from 0 to 1 in the north and up to 29 in the central part of the study areas [115]. A number of meteorological parameters are significantly correlated with the concentration of Alternaria spores in the Australia’s atmosphere, including average, minimum and maximum temperatures, dew point temperatures, and air pressure. Some of these meteorological values (average, minimum and maximum temperatures, dew point temperature) show significant correlations with a lag of 1, 2, and 3 days, as well as for the same day. Regression models show that up to 31.1% of the changes in the Alternaria spore concentration in this region can be explained by meteorological factors [103].

There is evidence that meteorological factors do not affect the concentration of Aspergillus/Penicillium spores. An increase in the concentration of spores of these species has been found in the evening and at night, when air humidity is usually higher [106].

Clouds, time of day, atmospheric pressure, and dew point temperature were also significant factors influencing Cladosporium spore concentration. The maximum abundance of Cladosporium spores in the air decreased between 12 and 17 hours [61,116]. A positive correlation (P < 0.02) was found between the concentration of Cladosporium spores and the average daily temperature, relative humidity, as well as a negative correlation with precipitation. A mathematical model has been developed for calculating Cladosporium spores using an annual seasonal cycle and significant weather variables [117]. Mantoani [118] found a doubling of the concentration of Cladosporium spores in the air with an increase in winter temperature in the Brazilian Atlantic forest, however, the observed biodiversity of fungi decreased.

The transport of spore by air masses movements, depending on the prevailing meteorological conditions, can be carried out at micro-, meso- (up to 100 km) and macroscales (more than 100 and up to thousands km). Surface and elevated inversions, cumulus and layered clouds play a certain role in the transport of spore masses (clouds), including phytopathogenic fungi, to different distances from the source. The transboundary transfer of rust uredospores from Greece, Bulgaria, Romania, Turkey and other countries in concentrations ranging from 0.9 to 80.3 units/m³ has been experimentally proven [119]. It was shown that the rotation of the Earth is one of the main factors in the spread of spores, which is amplified by the prevailing winds, using the example of the spread of spring wheat smut spores in the Urals. It is possible to monitor the phytosanitary situation and develop protective measures knowing the direction of the prevailing winds saturated with fungal spores [120]. The leading influence of prevailing winds in the transport of spores, primarily of rust and smut fungi, and the development of epiphytotics is indicated by a number of authors [119,121]. Earlier studies on the biogenic component of atmospheric aerosol in the south of Western Siberia showed that the sources located in Central Asia and Northwestern Kazakhstan have the greatest impact on the Siberian region [122]. The paper [123] indicate that the massive development of brown rust on spring wheat in Western Siberia is a consequence of the introduction of uredospores from winter crops in the southern regions of the European part of Russia. In recent years, a new aggressive strain of stem rust Ug 99 (Uganda 99) has been actively migrating towards the prevailing winds, and in the next 3-5 years it will be able to reach the states of Central Asia, from where the pathogen may be introduced into Western Siberia [124,125].

Gusty winds increase the spore content in the air of the genus Alternaria fungi, and the number of spores of the genus Cladosporium increases before rain [61,87,95].

3. Fungi in Atmospheric Aerosols of Western Siberia

Long-term studies of the fungal component of bioaerosol in the air of southern Western Siberia, conducted in 2001-2025, showed that the concentration of spores and the composition of fungi aerosol undergo seasonal and diurnal changes due to meteorological factors and its proximity to certain plants with clear seasonal dynamics, as well as with the specifics of the life cycles of the fungal species themselves [17,39,61,64,68,69,126,127].

A seasonal increase in the number of fungi in the air was observed in the spring-summer and early autumn periods, followed by a decrease in the late autumn period. The minimum number of fungi was observed in winter. In some years with an atypical warm winter for this region (2016), the presence of single spores of dark-colored fungi Aureobasidium, Penicillium in ground air samples in January was noted. In 2021, the appearance of sclerotic fungi was recorded in the south of Western Siberia, which were stably present in bioaerosol starting in April. Flour fungi, also not typical for previous years, were found in a number of samples starting in May 2021. Basidial fungi, which traditionally appear abundantly in August and September, have been isolated in small numbers from samples since April this year. These examples illustrate what was noted earlier in Kobzar [12]: global climate warming leads to changes in the quantitative and specific composition of spores in the aerosol; new species may appear in the region or there is a sharp increase in the level of existing fungal spores.

Гnpigmented isolates prevailed in the summer months, represented mainly by mycelial forms of fungi. By the end of the growing season, the proportion of pigmented isolates increases, including fungi of the genera Alternaria, Cladosporium, Penicillium, Trichoderma, as well as basidial and fusarium fungi, which is consistent with the seasonal dynamics of species, the abundance of which increases during the growing season [128].

The number of fungi in the summer months was also uneven in the samples taken using the Optical-E laboratory aircraft [129] at altitudes of 500-7000 m. Pigmented fungi (Alternaria, Cladosporium, Penicillium, Aureobasidium) prevailed here, which is consistent with the generally accepted opinion that the presence of pigments, especially melanin, in the cell membranes of fungi helps protect them from unfavorable factors, especially UV rays. Few spores were also observed during the winter months at altitudes from 1,500 to 7,000 m. Alternaria spores were found mainly at an altitude of 500 m, Fusarium spores reached a height of 1000 m. Aspergillus, Penicillium, and Cladosporium spores were recorded at all altitudes starting from 500 m. The species of the genera Microstoma, Sporobolomyces, Bullera, Aureobasidium, Sporidiobolus, Saccharmyces, cryptococcus, Candida, and Rhodotorula are represented among the yeasts and yeast–like fungi, which were especially abundant in April 2014 in high-altitude (0.5 - 2.0 km) atmospheric air samples [130]. These results are consistent with the available data that the spores of the fungi Cladosporium and Penicillium are present in the atmosphere throughout the year, and their highest concentrations are found during summer and autumn [61,67,77,104,106,131,132].

The number of Penicillium spores in the air positively correlated with daily relative humidity, average temperature, and dew point, which confirms and agrees with the available literature data [97]. The data on the number of Penicillium spores in different seasons, obtained by us and other researchers, confirm the thesis about the influence of meteorological factors in a specific geographical area on the concentration of spores [133,134,135].

Our research confirms the available evidence also that Cladosporium fungi are the most common in the atmosphere [26,59,61,92,106,133,134,136,137,138,139].

The trend of long-term dynamics of the number of fungal spores during the day is an increase in their number in the morning, a decrease in the afternoon and a repeated increase in the evening.

There is evidence in the literature that the time of the daily maximum varies for spores of different groups. A number of fungi (in particular, Cladosporium and Alternaria) are characterized by a “diurnal type” of distribution of spore concentration in the air, with a maximum in the afternoon (from 12 to 18 hours), while for basidiospores it is the opposite, in the morning (from 2 to 9 hours) [3,68]. Diurnal variations in concentration are determined by the taxonomic position of the spores and their volatility. Concentrations of basidiospores and conidia of deuteromycetes and basidiomycetes exhibit similar diurnal variations [17]. No clear trend of a daily maximum was observed for spores of different taxonomic groups in our studies. The maximum concentration of Cladosporium spores in the surface air was reached in the evening hours, which is consistent with existing data [106]. It is known that higher concentrations of fungal propagules (including Aspergillus and Penicillium) are observed at midnight and early morning hours, which is explained by an active mechanism of their release induced by a high dew point and increased air humidity at dawn [139]. In our studies, a tendency towards a high number of spores in the early morning hours was observed, but a clear association of the indicated genera with this time of day was not found.

The data obtained during the study confirmed the idea that, to accurately calculate the concentration of viable propagules and fully capture the biodiversity of mycoflora, it is necessary to use different cultivation temperature regimes, including low-temperature conditions, which allow, in particular, the identification of psychrophilic species. Fungal abundance during cultivation at low positive temperatures (6 - 10 °C) was 1.33 - 4.2 times higher than during cultivation under standard conditions.

The authors’ long-term observations of the total concentration of fungi in the atmosphere of the south of Western Siberia and their intra-annual variability, averaged over the observation period, are presented in Figure 1 and Figure 2.

As follows from a comparison of the data presented in Figure 1 with previously published data for the total concentrations of culturable microorganisms in the same measurements [140], the concentration of culturable micromycetes decreases during the observation period by a significantly smaller amount than the total concentration of culturable microorganisms, and their share in the total concentration of culturable microorganisms, as noted above, is not large.

As for the intra-annual dynamics of changes in the concentrations of micromycetes in the atmosphere of the south of Western Siberia, they are practically identical in the amplitude of changes to those for the total concentrations of culturable microorganisms in the same measurements [140]. Consequently, the climate changes occurring over 25 years of observations have affected the bacterial component of atmospheric aerosol to a greater extent than its fungal one.

Overall, the results of the study of the fungal component in atmospheric aerosol in southern Western Siberia showed that the abundance of fungal spores in the air varies widely depending on the sampling location, season, and time of day. Moreover, the results of the study in southern Western Siberia are quite comparable with those for other regions of the world, where bacteria predominate among the microorganisms in atmospheric aerosol.

4. Conclusions

This review demonstrates that the most significant parameters affecting the concentration of micromycetes in atmospheric aerosols are temperature, dew point, relative humidity, and wind speed. Average air temperature not only significantly influences the abundance of micromycetes in the air but also accelerates the onset of spore-producing seasons, which are determined by meteorological conditions by more than 40%. The sensitivity of moisture-loving and dry-spore-producing micromycetes to weather changes exhibits statistically significant differences.

A study of the fungal component in atmospheric aerosol in southern Western Siberia revealed wide variations in the abundance of fungal spores in the air depending on the sampling location, season, and time of day. And it should be noted that the results of the study in southern Western Siberia are quite comparable with those for other regions of the world, where bacteria predominate among the microorganisms in atmospheric aerosol.