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Original Articles

The variation in spore concentrations of selected fungal taxa associated with weather conditions in Szczecin, Poland, 2004–2006

Pages 139-146 | Received 12 Nov 2007, Accepted 28 Mar 2008, Published online: 12 Sep 2008

Abstract

The investigation of airborne fungal spore concentrations was carried out in Szczecin, Poland between 2004 and 2006. The objective of the studies was to determine a seasonal variation in concentrations of selected fungal spore types due to meteorological parameters. The presence of spores of ten taxa: Cladosporium, Ganoderma, Alternaria, Epicoccum, Didymella, Torula, Dreschlera‐type, Polythrincium, Stemphylium and Pithomyces was recorded in Szczecin using a volumetric method (Hirst type). Fungal spores were present in the air in large numbers in summer. The highest concentrations were noted in June, July and August. The peak period was recorded in August for most of the studied spore types: Ganoderma, Alternaria, Epicoccum, Dreschlera‐type, Polythrincium and Stemphylium. Cladosporium and Didymella spores reached their highest concentrations in July while concentrations of Torula were highest in May and Pithomyces in September. Multiple regression analysis was performed for three fungal seasons: 2004, 2005, and 2006. Spore concentrations were positively correlated with minimum temperature for seven spore types in 2004, for five spore types in 2005, and for eight spore types in 2006 (significance level of α = 0.05). Some spore types are also significantly correlation among their concentrations, pressure, relative humidity and rain. Minimum temperature appeared to be the most influential factor for most spore types.

The atmosphere contains a tremendous diversity of airborne spores with high concentrations frequently occurring from spring through fall in temperate areas of the world (Gregory, Citation1973).

It is well known that fungi require certain optimum conditions for each phase of their growth. In this regard, associations with temperature and moisture have been well documented in the mycological literature. It has been also established that spore concentrations in the atmosphere fluctuate with weather. Temperature, humidity, and rainfall also play important roles. However, airspore levels also vary for biological reasons, such as growth and differentiation of spores‐ or pollen producing organs (Gregory, Citation1973).

Fungi are able to grow at a relative humidity (RH) below that of bacteria and algae. The competitive ability of fungi is facilitated by its ability to respond by sporulating when the RH decreases. The minimum RH permitting growth varies between 75 and 95% for different species of mould (Gravesen, Citation1979).

The fungi are mainly mesophilic and optimal temperature for growth is 20–40°C, Some fungi (e.g., certain Cladosporium species) are psychrophilic (optimum below 20°C), and cause serious problems in refrigerated food storage (Gravesen, Citation1979).

In contrast to bacteria and algae, fungi are entirely heterotrophic. Their food demands range over a broad spectrum of organic material (Gravesen, Citation1979).

The knowledge of the composition of airborne spores of a particular area is important in agriculture because crop pathogens can be identified to help prevent crop epidemics and because some spores contribute to respiratory allergy in susceptible individuals. The characteristic features and size of the spores determine how deep they may penetrate into respiratory tract, whereby the exact site of allergic response can be determined. Spores larger than 10 µm diameter are deposited in the nasopharynx causing rhinitis; spores smaller than 5 µm penetrate to the alevoli causing alevolitis. Spores <10 µm size mostly deposit in the bronchi and bronchioles causing asthma (Lacey, Citation1996). The present study was conducted to determine the potential influence of different meteorological factors on the various fungal components of the airspora of the Szczecin region.

Material and methods

The analysis of the spore count and spore fall distribution was performed based on data collected in Szczecin in 2004–2006. The air sampling was carried out using a VPPS Lanzoni 2000 Spore Trap (Italy), set for seven day sampling onto Melinex tape. The sampler was located 21 m above ground level and approximately 5 km from the city center (Figure ). Sampler drums were changed weekly and the tapes cut into 48 mm segments, representing the previous 7 days. Concentrations are presented as spores per cubic meter of air.

Figure 1. The locality of the monitoring site at Natural Science Faculty of Szczecin University, see white square frame(149 m a. s. l.; 53°26′26″N, 14°32′50′′E), and the Meteorological Station Szczecin/Dabie ‐ black square frame. [Adapted p.p. from on‐line: MultiMap/Collins Bartholomew Ltd 2004.]

Figure 1. The locality of the monitoring site at Natural Science Faculty of Szczecin University, see white square frame(149 m a. s. l.; 53°26′26″N, 14°32′50′′E), and the Meteorological Station Szczecin/Dabie ‐ black square frame. [Adapted p.p. from on‐line: MultiMap/Collins Bartholomew Ltd 2004.]

The spore data were analysed to determine the start, end and duration of the season using the 90% method. The start of season was defined as the date when 5% of the seasonal cumulative spore count was trapped and the end of the season as the date when 95% of the seasonal cumulative spore count was reached.

The meteorological data for the three years were provided by the meteorological station in Dąbie borough of Szczecin and by the Automatic Weather Station (Vaisala, Finland). The meteorological parameters considered in the assessment of the effect of meteorological conditions on the airborne fungal spores were: daily level of precipitation, wind speed, relative humidity and air temperature.

The statistical relationship between spore concentration and meteorological factors was established using the Statistica program version 6.1 (StatSoft Inc., Citation2002).

Results

The cumulative annual and monthly totals of average daily concentrations of ten selected spore types are shown in Table .

Spores were present in large numbers throughout the summer with the highest levels being reached in May, June, July, August and September. Peak levels for Ganoderma, Alternaria, Epicoccum, Dreschlera‐type, Polythrincium and Stemphylium, were recorded in August; Cladosporium and Didymella spores reached their highest concentrations in July while concentrations of Torula were highest in May, and Pithomyces in September (Table ).

The least fluctuations for most spores were observed in 2005. The season started in June and July (only for Torula in March) and finished in September (Dreschlera‐type and Stemphylium) and October. For the most spore types, the duration of the season was the shortest when compared with 2004 and 2006. The annual totals of the daily concentrations were the highest for six spore types and are summarized in Tables and . For most spore types, the day of highest concentration occurred approximately in the middle of the season, except for Torula, for which the highest concentrations occurred in May (Table ).

Table I. Descriptive statistics of selected spore types in Szczecin (2004–2006).

Table II. Annual and monthly totals of the average daily concentrations of selected spore types in Szczecin (2004–2006).

Multiple regression analysis was performed in order to determine which meteorological variables were associated with spore concentrations. Meteorological data used in the multiple regression analysis included minimum temperature, relative humidity, rainfall and pressure. These variables correlated the strongest with spore concentrations (Table ). Other factors (average temperature, wind speed and direction) showed a slight to insignificant correlation. During 2004, the analysed season of spore concentration was positively correlated with minimum temperature for seven spore types (Cladosporium, Ganoderma, Alternaria, Epicoccum, Didymella, Torula and Dreschlera‐type), in 2005 for five spore types (Cladosporium, Ganoderma, Alternaria, Epicoccum, Didymella) and in 2006 for eight spore types (Cladosporium, Ganoderma, Alternaria, Epicoccum, Didymella, Torula, Dreschlera‐type and Stemphylium) (Table ). We also found that pressure significantly and negatively correlated with concentrations of six spore types in one of the seasons studied. The concentration of Alternaria, Torula, Dreschlera‐type and Polythrincium was significantly and negatively correlated with relative humidity in 2004 and Alternaria in 2006 (Table ).

Table III. Fungal spore concentration vs. meteorological factors in multiple regressions models in Szczecin (2004–2006).

The significant correlation between spore concentration and rain occurred only for two spore types. The positive correlation was noted for Didymella in 2004 and 2006 and negative for Ganoderma in 2005 and 2006. For the other spore types, the correlation with rain was not statistically significant in every analysed period (Table ).

Based on the results, we can conclude that the airborne fungal spores occur in Szczecin nearly throughout the whole year. Spore concentrations in the spring, late autumn and winter are low. Maximum spore concentrations occur in the summer and Cladosporium is the most frequently observed taxon. In January, February, March and December concentrations of Cladosporium conidia are usually low. Their maximum concentration is observed in July and August. The maximum concentration of the other spore types usually occurs in July and August. However, the values differ dramatically.

It is not certain that all variation in spore concentrations can be explained only by meteorological variables. Spore concentrations may also depend on the state of the host and the weather. The increase in fungal spore concentrations may be related to the maturing of tree foliage, grasses and local crops.

Discussion

The taxa chosen for analysis belong to the group of anamorphic fungi (also called conidial or mitosporic), except for Ganoderma (Basidiomycotina) and Didymella (Ascomycotina). The selection of taxa was arbitrary and it cannot be concluded that anamorphic fungi dominate the spectrum of airborne spores. Numerous papers confirm their high frequency and concentration in the air. However, according to many authors, airborne Basidiomycotina spores are equally common (Adams, Citation1964; Calderon et al., Citation1995; Diaz et al., Citation1998; Kasprzyk et al., Citation2004; Mitakakis & Guest, Citation2001; Stępalska & Wołek, Citation2005).

Szczecin is similar to the other cities in Poland (Kasprzyk et al., Citation2004; Konopińska, Citation2004; Myszkowska et al., Citation2002; Stępalska et al., Citation1999) and cities in Europe (Adams, Citation1964; Nikkels et al., Citation1996), in that the maximum spore concentrations of most taxa occur in July and August.

Cladosporium spores had the highest concentration in the seasonal spore count. The dominance of this genus over other spores has been observed in many locations, including Denmark (Larsen, Citation1981; Larsen & Gravesen, Citation1991), Spain (Infante & Dominquez, Citation1988; Infante et al., Citation1992), Italy (Cosentino et al., Citation1990; Marchisio et al., Citation1997), Austria (Ebner et al., Citation1992), Jordan (Shaheen, Citation1992), Sweden (Hjelmroos, Citation1993), India (Chakraborty et al., Citation2003; Singh et al., Citation1994), Canada (Li & Hsu, Citation1995), Finland (Kurkela, Citation1997), Australia (Mitakakis et al., Citation1997; Mitakakis & Guest, Citation2001) and in some stations in the United States (Sneller & Roby, Citation1979). However, in the United States, various surveys have reported Alternaria more frequently than other mould (except on the Pacific Coast where this taxon was found only sporadically or in reduced numbers (Prince & Meyer, Citation1976).

Alternaria, a common saprophyte through the world, is often found growing together with Cladosporium (Gravesen, Citation1979). Alternaria spore levels are relatively high compared to most other spore types and their numbers were highest during July and August. The highest numbers of Alternaria spores are usually encountered during the summer in Poland (Gaweł et al., Citation1996; Kasprzyk et al., Citation2004; Konopińska, Citation2004; Stępalska & Wołek, Citation2005), Denmark (Larsen & Gravesen, Citation1991) and Sweden (Hjelmroos, Citation1993).

Contrary to these results in Amman, Jordan the maximum Alternaria spore counts were recorded in October because of wet and warm conditions (Shaheen, Citation1992).

The minimum temperature was the most important meteorological factor associated with most of analysed spore types. Every type of fungal spore had a positive, significant correlation with Tmin during at least one season (except Polythrincium). In 2004 the correlation was noted for seven spore types, in 2005 for five and in 2006 for eight.

The strongest correlation during the seasons studied was noted for Cladosporium, Alternaria, Ganoderma, and Epicoccum in 2004; for Cladosporium, Alternaria, and Ganoderma in 2005; and for Cladosporium, Alternaria, Dreschlera‐type and Stemphylium in 2006. The positive, significant correlation between spore count and minimum temperature for Cladosporium, Dreschlera‐type and Stemphylium was noted in Cracow by Stępalska and Wołek (Citation2005). The correlation between Alternaria spore count and minimum temperature was not significant. Fernandez et al. (Citation1998) observed an increase of Cladosporium spore levels at a minimum temperature above 13°C in summer.

The second influential variable for the majority of selected spore types in analysed periods was air pressure. The negative, significant correlation was noted for six spore types but only in one from three studied seasons. Hjelmroos (Citation1993) noted the same statistically insignificant results for Cladosporium and Alternaria in Sweden.

Four spore types (Alternaria, Torula, Dreschlera‐type and Polythrincium) had negative and significant correlation with relative humidity in one season (2004). Alternaria showed a similar negative and significant correlation in 2006. Hjelmroos (Citation1993) and Stępalska & Wołek (Citation2005) noted increasing spore count in the air with increasing relative humidity. Hjelmroos (Citation1993) studied (ten year period) the relationship of Cladosporium and Alternaria to weather parameters using a statistical model. None of the meteorological parameters had significant canonical coefficients and no statistical model was proposed for Alternaria.

In our study Didymella was the second spore type for which the highest number of spores was noted. Its spore release may be triggered by local weather conditions, i.e., rainy period preceded by temperature above 20°C (Corden & Millington, Citation1994). Such conditions occurred in July and August when the high maximum temperature were followed by heavy rainfall. In the present study the highest counts of Didymella spores were found during this period. Results of multiple regression analysis suggest that precipitation is the most influential factor only for Didymella spore types during studied period. Since in ascomycetes water is needed to expel the spores, the positive, significant correlation between precipitation and Didymella spore count was noted in two of the three analysed seasons (2004 and 2006).

Ganoderma basidiopores occurred frequently together with Cladosporium and Alternaria in Szczecin. Seasonally, spore levels of Ganoderma peaked toward summer and autumn. Tarlo et al. (Citation1979) found Ganoderma basidiospores to be the most prevalent fungal airborne fungal spores in Canada. Studies from New Zealand also reported that Ganoderma basidiospores constituted a major component of the airspora (Hasnain et al., Citation1984, Citation1985; Cutten et al., Citation1988; Hasnain, Citation1993). Ganoderma has been reported as an important and prevalent fungal airspora component worldwide (Halwagy, Citation1994; Hasnain, Citation1993; Hasnain et al., Citation1984, Citation1985; Herxheimer et al., Citation1969; Lehrer et al., Citation1986, Citation1994; Levetin, Citation1990, Citation1991; Li & Kendrick, Citation1994, Citation1995; Mitakakis & Guest, Citation2001; Stępalska & Wołek, Citation2005). Gregory and Hirst (Citation1952) first suggested that basidiospores might be associated with allergy. Ganoderma basidiospores have subsequently been reported as having allergenic properties (Lehrer & Horner, Citation1990; Vijay et al., Citation1991) and have been implicated in the elicitation of respiratory allergic diseases (Cutten et al., Citation1988).

From all analysed spore types, only Ganoderma (in two seasons in 2005 and 2006) had negative, statistically significant correlation with rainfall. The same results were noted by Hasnain (Citation1993) in Auckland (New Zealand) and in Cracow by Stępalska and Wołek (Citation2005).

The spore types that showed the fewest correlations with meteorological factors were Stemphylium and Polythrincium. Pithomyces did not show any correlation to meteorological factors. These three spore types also had the lowest annual and monthly concentrations during all studied seasons. Mitakakis and Guest (Citation2001) noted the similar results for these spore types in Melbourne (Australia). The percentage contribution of Stemphylium, Polythrincium and Pithomyces in 1993 was 0.2; 0.3; and 0.4, respectively. The highest number of spores for these three spore types occurred in summer like for the most analysed spore types.

The summer peak in spore concentrations might be obtained by favourable temperature and also air pressure and humidity. In late summer and autumn still high level of spore counts may be explained by the beginning process of seasonal decay of vegetable matter. The low spore frequency in the winter months is probably due to the snow cover, but the spore frequencies start decreasing already in November before snowfall, when the temperature falls below zero preventing sporulation.

This study only describes the part of microfungal flora in a restricted area, and further study is required in order to evaluate the effects of local vegetation and climate on the fungal flora.

Conclusions

Spores of the studied fungal taxa were collected in the air almost year‐round yet daily spore concentrations varied considerably. The maximum spore concentration of most taxa occurred in July and August, and their concentrations exceeded threshold values provoking allergy symptoms from June to September. In the three‐years analysed, the minimum temperature was the most important factor correlating significantly and positively with the concentration of the majority of spores.

Acknowledgements

Research financed by KBN Grant No. 2, P04G 099 29 in the years 2005 and 2006.

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