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Fungal spores are an important cause of allergic respiratory diseases worldwide. However, little is known about the intradiurnal pattern of spore concentrations of different fungal spore types in the air of the urban area. In this study, we evaluated bihourly variation in spore concentration of eight predominant fungal spore types in the atmosphere of Bratislava city (Agrocybe, Alternaria, Cladosporium, Coprinus, Exosporium, Epicoccum, Ganoderma, Leptosphaeria) with the aim to understand the relationships between the spore concentrations against associated environmental variables. Spore samples were collected using a Hirst-type volumetric aerospore trap from January to December 2016. Alternaria, Cladosporium, Epicoccum and Exosporium peaked during the daytime period between 10:00 and 16:00, while for Agrocybe, Ganoderma, Coprinus and Leptosphaeria, the nighttime peaks (20:00 and 04:00) were observed. Effect of a complex of environmental variables on bihourly concentrations of selected airborne fungal spore taxa was evaluated through multiple regression analysis. Air temperature, wind speed, sunshine duration and precipitation were positively associated with daytime spore types, while the association with nighttime spores was negative. In contrast, relative air humidity influenced negatively Exosporium daytime spore type but positively the Leptosphaeria nighttime spore type. Moreover, a circadian cycle of light and darkness was considered as an important predictor of nighttime spore levels. Among the atmospheric pollutants, PM10 was positively associated with all analysed daytime spores, while except for Leptosphaeria, O3 was negatively associated with nighttime spore types. NO2 and PM10 had mixed effects on nighttime spore levels. In general, air temperature, PM10 and wind speed were environmental parameters with great influence on airborne fungal spore concentration, being present in eight, seven and four regression models, respectively. Constructed regression models which the best explained variation in fungal spore concentrations were those for Ganoderma (R² = 0.38) and Alternaria (R² = 0.31).
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RESEARCH ARTICLE
Intradiurnal variation of predominant airborne fungal spore
biopollutants in the Central European urban environment
Jana Ščevková
1
&Michal Hrabovský
1
&Jozef Kováč
2
&Samuel Rosa
2
Received: 22 April 2019 /Accepted: 25 September 2019
#Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Fungal spores are an important cause of allergic respiratory diseases worldwide. However, little is known about the intradiurnal
pattern of spore concentrations of different fungal spore types in the air of the urban area. In this study, we evaluated bihourly
variation in spore concentration of eight predominant fungal spore types in the atmosphere of Bratislava city (Agrocybe,
Alternaria,Cladosporium,Coprinus,Exosporium,Epicoccum,Ganoderma,Leptosphaeria)withtheaimtounderstandthe
relationships between the spore concentrations against associated environmental variables. Spore samples were collected using
a Hirst-type volumetric aerospore trap from January to December 2016. Alternaria,Cladosporium,Epicoccum and Exosporium
peaked during the daytime period between 10:00 and 16:00, while for Agrocybe,Ganoderma,Coprinus and Leptosphaeria,the
nighttime peaks (20:00 and 04:00) were observed. Effect of a complex of environmental variables on bihourly concentrations of
selected airborne fungal spore taxa was evaluated through multiple regression analysis. Air temperature, wind speed, sunshine
duration and precipitation were positively associated with daytime spore types, while the association with nighttime spores was
negative. Incontrast, relative air humidity influencednegatively Exosporium daytime spore type but positively the Leptosphaeria
nighttime spore type. Moreover, a circadian cycle of light and darkness was considered as an important predictor of nighttime
spore levels. Among the atmospheric pollutants, PM
10
was positively associated with all analysed daytime spores, while except
for Leptosphaeria,O
3
was negatively associated with nighttime spore types. NO
2
and PM
10
had mixed effects on nighttime spore
levels. In general, air temperature, PM
10
and wind speed were environmental parameterswith great influence on airborne fungal
spore concentration, being present in eight, seven and four regression models, respectively. Constructed regression models which
the best explained variation in fungal spore concentrations were those for Ganoderma (R
2
= 0.38) and Alternaria (R
2
=0.31).
Keywords Fungal spores .Weather p arameters .Aerobiology .Aeroallergen .Air pollutants .Regression analysis
Introduction
Fungal spores, the reproductive or distributional structures
produced during the life cycle of fungal organisms, are very
numerous in the air (Kasprzyk 2008). They can have severe
economic impacts through the spread of plant diseases (Rossi
et al. 2005) and biodeterioration of art sculptures or architec-
tural pieces (Caneva et al. 2003). Moreover, some of them are
known as natural aeroallergens that may cause allergic respi-
ratory diseases in sensitive individuals (DAmato and
Spieksma 1995). According to Yamamoto et al. (2012), 2.8
10.7% of total airborne spore types are considered as allergen-
ic. The prevalence of spore-induced allergic reactions has
been increasing worldwide during the past several decades
and is estimated to be approximately 10% of the worldspop-
ulation which is allergic to spores of fungal organisms (Maio
et al. 2011).
Although the quantity of fungal spores in the air varies both
throughout the season and day, the published literature refers
mainly to seasonal variability. Much fewer researchers
worked on the intradiurnal pattern (Stępalska and Wołek
2009; Oliveira et al. 2009; Grinn-Gofrońet al. 2018).
However, information concerning high allergy risks during
Responsible Editor: Philippe Garrigues
*Jana Ščevková
jana.scevkova@uniba.sk
1
Faculty of Natural Sciences, Department of Botany, Comenius
University, Révová 39, 811 02 Bratislava, Slovakia
2
Faculty of Mathematics, Physics and Informatics, Department of
Applied Mathematics and Statistics, Comenius University, Mlynská
dolina, 842 48 Bratislava, Slovakia
Environmental Science and Pollution Research
https://doi.org/10.1007/s11356-019-06616-7
the daily hours would be helpful for allergy sufferers to plan
outdoor activities because allergy symptoms often culminate
with the peak spore concentrations (Lin et al. 2016).
Intradiurnal variations of airborne fungal spores depend,
among others, on weather conditions which affect the sporu-
lation, dispersal and deposition of spores. Based on their oc-
currence in the air during different weather conditions, fungal
spores are divided into two groups, dryand wetspore
types. Dry spores (xerophilic) are found in the greatest abun-
dance in the air under conditions of decreasing humidity and
increasing airflow (Elbert et al. 2007). On the other hand, wet
spores (hydrophilic), belonging to Ascomycetes and
Basidiomycetes, are released from sporangium into the atmo-
sphere by processes related to humidity conditions or rain
(Horner 1992).
During the daily hours, the distribution of airborne spores
may also be influenced by air pollutants, including particulate
matter with an aerodynamic diameter 10 μm(PM
10
), ozone
(O
3
), nitrogen dioxide (NO
2
) and carbon monoxide (CO) as it
may interact with the atmospheric processes and affects the
weather conditions (Pyrri and Kapsanaki-Gotsi 2017).
However, the impact of air pollutants on airborne fungal
spores has been rarely considered (Lin and Li 2000;Ho
et al. 2005; Sousa et al. 2008;Grinn-Gofrońet al. 2011).
In Slovakia, little attention has been paid to outdoor air-
borne spores of fungal organisms. Although the seasonal dis-
tribution of fungal spores has previously been investigated in
Bratislava (Chrenová et al. 2004;Ščevková et al. 2016;
Ščevková and Kováč2019), their intradiurnal distribution
was not studied in this country at all. Therefore, this study
aims at presentation of an intradiurnal pattern of the spore
concentrations of eight predominant allergenic spore types in
the air of Bratislava and examination of the environmental
parameters that had the greatest impact on the pattern. The
result of this study could be useful for clinicians and allergy
sufferers, in order to define preventive avoidance strategies.
Moreover, this study could also be useful for farmers in order
to avoid economic losses due to fungal plant diseases by cor-
rect timing of the application of fungicides.
Materials and methods
Study area
Bratislava, the capital of Slovakia, is a city of around 430,000
inhabitants with about 1164 persons/km
2
density. Bratislava is
located in the south-western part of Slovakia (Fig. 1)onthe
boundary between the Malé Karpaty Mountains and the
Pannonian Lowland. The river Danube flows through the mid-
dle of the city. The landscape of its surroundings isconstituted
by farmland areas (mainly cereal fields and vineyards) and
deciduous Carpathian forests dominated by Quercus spp.,
Carpinus betulus L. and Fagus sylvatica L. and alluvial for-
ests dominated by Ulmus spp., Fraxinus spp., Salix spp. and
Populus spp., among others. Its climate is temperate continen-
tal with warm summers and cold winters. In 2016, mean an-
nual temperature was 11.1 °C. The coldest month was January
(mean 0.2 °C) and the warmest was July (mean 21.6 °C).
Over the study period, the total precipitation was 776.4 mm,
with the maximum value in July (137.1 mm) and the mini-
mum value in December (12.1 mm).
Aerobiological data
Airborne fungal spores were collected from January to
December 2016 by using Burkard 7-day volumetric aerospore
sampler, placed on the roof of the Department of Botany,
Faculty of Natural Sciences building (48° 0846N, 17° 04
43E, 157 m a. s. l.), in the north-west part of the city at 10 m
above ground level. This area is surrounded by urban vegeta-
tion, mainly by ornamental trees and shrubs cultivated in the
parks and gardens and by vegetation along footpaths, roads
and buildings. Botanical garden and Danube River are located
in the vicinity. Single-family houses are the dominant building
types. The methodology used was performed according to the
standard method adopted by the British Aerobiology
Federation (1995). Air is suctioned into the sampler through-
out a horizontally orientated 2 × 14 mm slit at a rate of 10 l/
min and impacted against an adhesive tape that moves contin-
uously pastthe slit at a rate of 2 mm/h.The sampling tape was
changed weekly at 10:00 (local timeUTC + 2 h in the sum-
mer, UTC + 1 h in the winter). The tapes were cut into seg-
ments 48 mm long, each representing 24 h exposure, and were
mounted on microscope slides in gelatin-glycerin and stained
with basic fuchsin. Spores were counted in 12 transversal
traverses per slide under a light microscope at a magnification
of × 400. After the spore counting in each sampling area, a
specific correction factor for the used microscope was applied.
Results were expressed as bihourly average spore concentra-
tions per cubic metre of air (spores/m
3
).
Meteorological and air pollution data
To analyze the effect of meteorological parameters on the
intradiurnal spore concentrations, bihourly records of follow-
ing meteorological variables were taken into consideration:
Tsurface air temperature (°C), RHrelative air humidity
(%), Pprecipitation (mm), WSwind speed (m/s), S
sunshine duration (h) and APatmospheric pressure (hPa).
Meteorological data were recorded at the meteorological ob-
servatory of the Department of Astronomy, Physics of the
Earth and Meteorology of the Faculty of Mathematics,
Physics and Informatics (48° 0904N, 17° 0414E, 182
m a. s. l.) situated 1 km NW of the sampling site.
Environ Sci Pollut Res
Bihourly records of atmospheric pollutants, PM
10
partic-
ulate matter 10 μm(μg/m
3
), O
3
ozone (μg/m
3
), NO
2
nitrogen dioxide (μg/m
3
) and COcarbon monoxide (μg/
m
3
), were obtained from the database of the Slovak
Hydrometeorological Institute (SHMÚ), which has four air
quality monitoring stations throughout Bratislava. The data
used in the analysis were calculated as an average of data
obtained from all four air quality monitoring stations.
Data analysis
Analysis of bihourly mean spore concentrations was per-
formed for eight fungal taxa: Alternaria,Cladosporium and
Epicoccum of Deuteromycetes; Agrocybe,Coprinus and
Ganoderma of Basidiomycetes; and Exosporium and
Leptosphaeria of Ascomycetes. These taxa were selected ac-
cording to allergenic capacity and their high-level presence in
the air of Bratislava.
The analysis of the intradiurnal variation in airborne spore
concentration was performed during the main spore season
(MSS) for each spore type (Table 1). MSS has been calculated
following the methodology designed by Nilsson and Persson
(1981). This method includes 90% of the seasonal total spores
and comprises from the day in which 5% of total spores is
registered to the day in which 95% of total spores is registered.
The following time intervals were selected to reflect air-
borne spore levels during day and night: 08:0020:00 (equiv-
alent of daytime, 12 h) and 20:0008:00 (equivalent of night-
time, 12 h).
The effects of the environmental variables on the airborne
spore concentration of selected fungal taxa were analysed
using linear regression models in the statistical software R
(version 3.5.2). An indicator variable for daytime/nighttime
period and its interactions with relative air humidity and air
temperature were added to the models to cover potential ef-
fects of the circadian cycle of light and darkness. To correct for
autocorrelation of the measurements, autoregressive
moving average (ARMA) correlation structure was selected
for the models by using the function gls from the nlme pack-
age. The autoregressive and the moving average orders were
determined automatically by the function auto.arima from the
forecast package applied on the residuals of the regression
model that did not allow for correlation in the observations.
For each fungal taxon, a regression model containing all
Table 1 Characteristics of the main spore seasons of selected fungi taxa
in the air of Bratislava, in 2016
Fungal taxa Characteristics*
SS SL Max
Agrocybe 12 May13 Nov 186 306 (27 Octo)
Alternaria 25 June17 Octo 115 908 (26 July)
Cladosporium 14 May1 Nov 172 13,812 (17 July)
Coprinus 22 April29 Octo 191 1100 (27 July)
Epicoccum 22 June20 Nov 152 231 (23 Octo)
Exosporium 28 May30 Sept 126 210 (24 June)
Ganoderma 19 June1 Octo 105 644 (3 Sept)
Leptosphaeria 2June20 Octo 141 1541 (28 July)
*SS start and end dates, respectively; SL length of spore season; and Max
maximum daily mean spore concentrations (spores/m
3
)anditsdate(in
parenthesis)
Fig. 1 Localization of Bratislava in Slovakia
Environ Sci Pollut Res
considered explanatory variables was fitted and insignificant
variables (pvalue > α, where the significance level αis 0.05)
were sequentially removed from the model by using likeli-
hood ratio tests. Note that pvalues for some variables are
above 0.05 in Table 2. However, the removal of any of these
variables would result in significant loss of information com-
pared to the model with all explanatory variables (pvalue <
0.05); therefore, they were retained in the final models.
Results
The intradiurnal evolution of the levels of meteorological and
air pollution parameters in Bratislava during the study period
based on the bihourly evolution is presented in Figs. 2and 3.
The intradiurnal trend ofair temperature pointed out a gradual
increase during the morning, remaining high during noon and
early afternoon and then gradually decreasing until the pre-
dawn. Relative air humidity remains between 60 and 70%
from noon to early evening, while throughout the rest daily
hours, relative air humidity remains between 70and 85%.The
intradiurnal variations of wind speed and sunshine duration
showed a similar pattern with the highest values at noon and
the lowest values between 20:00 and 04:00. The maximum air
pressure was observed at 08:00, whereas higher precipitation
was observed between 20:00 and 06:00. Taking into account
air pollutants, the highest PM
10
and O
3
concentrations were
observed at 10:00 and 14:00, respectively, while during the
early morning hours, the minimum concentrations of two
above-mentioned air pollutants were observed. The high con-
centrations of CO and NO
2
were observed both in the early
evening (16:0018:00) and early morning (06:0008:00)
hours.
The study of an intradiurnal periodicity of fungal spore
concentrations was performed for eight allergenic fungal taxa
(Agrocybe,Alternaria,Cladosporium,Coprinus,Epicoccum,
Exosporium,Ganoderma and Leptosphaeria) occurring in
high numbers in the air of Bratislava (Ščevková and Kováč
2019). The analysed taxa showed a pattern with differences
between the spore types and the bihourly distribution (Fig. 4).
We classified the airborne spores into two categories, daytime
(Alternaria,Cladosporium,Epicoccum,Exosporium)and
nighttime (Agrocybe,Coprinus,Ganoderma,Leptosphaeria)
spore types depending on their releasing pattern.
Cladosporium and Exosporium show the highest amount of
spores in the morning at 10:00, with 64.0 and 68.3% of spores,
respectively distributed between 08:00 and 18:00. Epicoccum
reaches its maximum at noon, with 47.3% of spores distribut-
ed between 10:00 and 16:00. During the daytime (10:00
18:00), the amount of Alternaria spore registered is 55.8%,
with a peak in the afternoon at 16:00. All four above-
mentioned daytime spore types reach the minimum at mid-
night. Agrocybe,Ganoderma,Coprinus and Leptosphaeria
nighttime spore types show their maximum spore concentra-
tions at nighttime. Agrocybe and Ganoderma concentrate 61.5
and 67.8% of spores, respectively between 18:00 and 04:00,
showing the maximum at 20:00, with a second peak at 04:00.
Coprinus and Leptosphaeria show a peak at 04:00 and con-
centrate 64.7% of spores between 20:00 and 06:00 for
Coprinus and 50.9% of spores between 02:00 and 08:00 for
Leptosphaeria.Moreover,Coprinus reaches a second peak at
22:00. Agrocybe,Ganoderma and Coprinus reach the mini-
mum in the afternoon at 14:00, while Leptosphaeria shows
the lowest amount of spores at 20:00 (Fig. 4).
Table 2shows the results of multiple regression analysis,
which was performed in order to identify the environmental
variables which the most influenced airborne fungal spore
concentrations. The results revealed that meteorological pa-
rameters were important determinants of fungal spore concen-
trations and that air temperature, wind speed, sunshine dura-
tion and precipitation were the most consistent predictors for
fungal spore levels of daytime spore types. Air temperature
was positively associated with all analysed dry spore types,
whereas wind speed, sunshine duration and precipitation were
positively associated only with some of them. Wind speed had
a positive association with Cladosporium and Exosporium,
sunshine duration was positively associated with Epicoccum
and Exosporium and precipitation had a positive association
with Alternaria and Cladosporium. Moreover, relative air hu-
midity and atmospheric pressure showed a significant
(negative) association with Exosporium and Alternaria, re-
spectively. On the other hand, the most consistent predictors
for spore concentrations of nighttime spore types were air
temperature, daytime interval and wind speed. Air tempera-
ture was negatively associated with all analysed wet spore
types, whereas daytime interval was negatively associated
with Agrocybe,Coprinus and Ganoderma. Relative air hu-
midity was positively associated with Leptosphaeria,while
the association with precipitation was negative. Wind speed
was negatively associated with Coprinus and Ganoderma.
Finally, the sunshine duration was negatively associated with
Ganoderma spore type in the multivariate models.
In addition to meteorological parameters, also several at-
mospheric pollutants were significantly associated with spore
concentrations (Table 2). Except for Coprinus and
Leptosphaeria, the spore concentrations of all analysed fungal
taxa increased with the increase in PM
10
levels. The spore
concentration of Coprinus and Cladosporium increased at
higher CO and NO
2
levels, respectively, whereas the concen-
tration of Agrocybe and Ganoderma increased at higher NO
2
levels. By contrast, PM
10
,O
3
and NO
2
were negatively asso-
ciated with Leptosphaeria,whileCoprinus and Ganoderma
were negatively associated with O
3
levels.
For Alternaria,Exosporium,Cladosporium and
Epicoccum daytime spore types, environmental parameters
explained 30.9, 14.0, 13.1 and 11.9% of the total variance,
Environ Sci Pollut Res
respectively, while for Ganoderma,Leptosphaeria,Agrocybe
and Coprinus nighttime spore types, environmental parame-
ters explained 38.1, 16.6, 13.0 and 5.8%, respectively
(Table 2).
Discussion
Analysis of intradiurnal variability in spore concentration of
eight analysed fungal taxa in the atmosphere of Bratislava
included in this study shows that peak concentrations for dry
spore types tended to be recorded during the daytime period,
whereas wet spores reached its peaks during the nighttime
period. Taking into account dry spore types, the greatest spore
concentrations occurred in the morning at 10:00 for
Cladosporium and Exosporium,atnoonforEpicoccum and
in the afternoon at 16:00 for Alternaria. The occurrence of the
highest spore values around midday between 10:00 and 12:00
is mainly related to huge spore emission due to favourable
weather conditions, such as high air temperature and wind
Table 2 Significant environmental variables in multiple regression models for selected fungal spore types in Bratislava
Spore type Variables βcoeff. Std. error pvalue R
2
Proportion of varianceexplained (%)
Agrocybe Intercept 4.2524 1.1609 0.0003 0.130 13.0
PM
10
(μg/m
3
) 0.0471 0.0148 0.0015
NO
2
(μg/m
3
) 0.0616 0.0096 < 0.0001
Temperature (°C) 0.1456 0.0276 < 0.0001
Daytime 0.7964 0.1919 < 0.0001
Alternaria Intercept 552.2548 271.9856 0.0425 0.309 30.9
PM
10
(μg/m
3
) 0.4889 0.0645 < 0.0001
P(hPa) 0.5702 0.2727 0.0367
Precipitation (mm) 2.5919 0.4269 < 0.0001
Temperature (°C) 1.1143 0.1126 < 0.0001
Cladosporium Intercept 547,892 66.7671 0.4120 0.131 13.1
PM
10
(μg/m
3
) 4.7143 0.9090 < 0.0001
NO
2
(μg/m
3
) 1.6827 0.7204 0.0196
CO (μg/m
3
)0.0836 0.0581 0.1508
Precipitation (mm) 10.4301 4.5455 0.0219
Temperature (°C) 12.6277 1.6148 < 0.0001
Wind speed (m/s) 18.1037 5.1227 0.0004
Coprinus Intercept 43.8255 7.2136 0.0001 0.058 5.8
O
3
(μg/m
3
)0.1955 0.0382 < 0.0001
CO (μg/m
3
) 0.0140 0.0046 0.0024
Wind speed (m/s) 2.0458 0.4713 < 0.0001
Temperature (°C) 0.5826 0.2170 0.0073
Wind speed (m/s) 2.0082 0.4749 < 0.0001
Daytime 0.4337 0.1704 0.0110
Epicoccum Intercept 0.3434 0.7764 0.6583 0.119 11.9
PM
10
(μg/m
3
) 0.0937 0.0180 < 0.0001
Temperature (°C) 0.0926 0.0316 0.0035
Sunshine (h) 1.2641 0.2843 < 0.0001
Exosporium Intercept 0.7955 1.4915 0.5939 0.140 14.0
PM
10
(μg/m
3
) 0.0627 0.0145 < 0.0001
Temperature (°C) 0.0771 0.0405 0.0570
Relative humidity (%) 0.0210 0.0104 0.0428
Wind speed (m/s) 0.1590 0.0852 0.0622
Sunshine (h) 0.7581 0.2088 0.0003
Ganoderma Intercept 32.4080 4.0332 < 0.0001 0.381 38.1
O
3
(μg/m
3
)0.1139 0.0301 0.0002
PM
10
(μg/m
3
) 0.3485 0.0934 0.0002
NO
2
(μg/m
3
) 0.3915 0.0451 < 0.0001
Temperature (°C) 0.5021 0.1656 0.0025
Wind speed (m/s) 2.1029 0.4133 < 0.0001
Sunshine (h) 5.1318 1.1539 < 0.0001
Daytime 5.2926 1.0126 < 0.0001
Leptosphaeria Intercept 12.2605 10.0619 0.2232 0.166 16.6
O
3
(μg/m
3
)0.1106 0.0457 0.0157
PM
10
(μg/m
3
)0.3742 0.1049 0.0004
NO
2
(μg/m
3
)0.1412 0.0641 0.0277
Temperature (°C) 0.9933 0.2768 0.0003
Precipitation (mm) 3.5145 0.6325 < 0.0001
Relative humidity (%) 0.3888 0.0735 < 0.0001
Environ Sci Pollut Res
speed accompanied by a low relative air humidity (Fig. 2).
Results similar to those obtained in Bratislava were found in
Cracow (Poland) (Stępalska and Wołek 2009) and Zagreb
(Croatia) (Peternel et al. 2004) where Cladosporium spore
concentrations were the highest between 10:00 and 12:00.
However, these results differ from those obtained by other
researchers who reported hourly peak Cladosporium concen-
trations between 12:00 and 14:00 in León (Spain) (Fernandez
et al. 1998), between 14:00 and 15:00 in Michigan (USA)
(Burge 1986) and even between 20:00 and 22:00 in Cordoba
(Spain) (Mediavilla et al. 1997). Such variability may be
explained by the differences in climate and biogeographical
characteristics of the areas under study. Likewise, in
Harpenden (UK), the highest Epicoccum spore concentrations
usually occurred towards the middle of the day around 11:00
(Sreeramulu 1959). However, these resultsare in contrast with
Jones and Harrison (2004) who concluded that extreme mid-
day conditions (high air temperature and low air humidity)
reduce concentrations of bioaerosols in the atmosphere.
Spores of Deuteromycetes (conidiospores) are released by a
passive mechanism or external forces (e.g., nearby wind cur-
rents). The most types of conidiospores grow in an exposed
Fig. 2 Intradiurnal evolution in
mean bihourly values of air
temperature (T), sunshine
duration (S), wind speed (WS),
relative air humidity (RH),
atmospheric preassure (AP) and
precipitation (P) in Bratislava in
2016
Fig. 3 Intradiurnal evolution in
mean bihourly values of
particulate matter 10 μm
(PM
10
), ozone (O
3
), carbon
monoxide (CO) and nitrogen di-
oxide (NO
2
) in Bratislava in 2016
Environ Sci Pollut Res
position and released inertly when disturbed. Therefore, the
rising of airborne conidiospore concentrations in the morning
could be attributed to the increase in wind speed after sunrise
as the wind causes vibrations that facilitate detachment of
spores and their release into the air (Rich and Waggoner
1962). Similarly to our results, Alternaria has previously been
described as afternoon taxon, with concentration peaks occur-
ring from noon to 21:00 (Munuera Giner et al. 2001;Oliveira
et al. 2009). This afternoon peaks could be related to a reduc-
tion of turbulence in the afternoon which allows spores to
settle. However, Munuera Giner et al. (2001) reported that
afternoon peaks can be induced by a delay in a sampling of
spores released earlier and being transported to the sampler
from remote sources. In the other study, a different result was
found from our study about intradiurnal variations of
Alternaria spores; in Stockholm (Sweden), maximum levels
were recorded in the morning at 08:00 (Hjelmroos 1993). The
lowest spore concentrations of all four analysed dry spore
types, similarly to other researchers (Bardei et al. 2017)oc-
curred at midnight, mainly due to unfavourable weather con-
ditions, such as low air temperature and wind speed accom-
panied by high relative air humidity (Fig. 2).
In Bratislava, just like in several other aeromycological
studies (Kasprzyk et al. 2004; Sánchez Reyes et al. 2016),
the greatest spore concentrations of wet spore types occurred
at night or in early morning hours when low air temperature
and wind speed were accompanied by high relative air humid-
ity (Fig. 2). This intradiurnal rhythm, in which the highest
abundance of spores presents between the night and early
morning period, suggests an active release mechanism in-
duced by increased air humidity prevalent at dawn. We have
recorded a double peak pattern for Agrocybe,Coprinus and
Ganoderma spore concentrations during a 24-h period. For
Agrocybe and Ganoderma, a greater peak appeared at night
at 20:00, and a second smaller peak appeared in the early
morning at 04:00. Similar results were obtained by Stępalska
and Wołek (2009) who found peak concentrations of
Ganoderma spores in the early morning hours between
02:00 and 04:00. For Coprinus, we have displayed double
peak pattern with a greater peak at 04:00, and second smaller
one occurring at 22:00, just like other surveys registered
(Antón et al. 2019). In our study, Leptosphaeria wet spores
were common at nighttime and reached the maximum values
in the early morning at 04:00, which could be due to high
relative air humidity during this daily hour.
Weather parameters are known to influence the production,
release and dispersal of fungal spores. In the present study,
results of multiple regression analysis showed air temperature
as the meteorological factor which significantly influenced the
concentration of all analysed spore types in the atmosphere of
Bratislava. The association with dry spores (Cladosporium,
Alternaria,Epicoccum and Exosporium) was positive, where-
as the association with wet spores (Agrocybe,Coprinus,
Ganoderma and Leptosphaeria) was negative. Likewise, ac-
cording to several other researchers (Peternel et al. 2004;
Kasprzyk et al. 2004), the air temperature was considered as
the most influential meteorological factor positively correlated
with the dry spore concentrations. This phenomenon is prob-
ably linked to the fact that, in order to be released into the air,
dry spores require a certain degree of dryness, which occurs
when the air temperature increases (Nolard et al. 2001).
Besides air temperature, wind speed was also a significant
factor explaining the variability in Cladosporium and
Exosporium spore concentrations, exhibiting a significant
Fig. 4 Intradiurnal variation in the spore concentration (SC) of major spore types in 2016, expressed in percentage
Environ Sci Pollut Res
and positive relationship with above-mentioned dry spore
types. Wind speed directly promotes the release of dry spores
and plays an important role in the spore dispersal.
Dry spores require less amount of humidity for sporulation
and, for this reason, their concentration is highest around mid-
day when the relative air humidity is low (Quintero et al.
2010). However, on the basis of our study results, it seems
that relative air humidity does not influence most of the air-
borne dry spore concentrations as the significant and negative
association was only observed with Exosporium.
The association between dry spores and precipitation are
not always the same. Contrary to results obtained by other
researchers (Martínez Blanco et al. 2016; Ianovici 2016),
who observed a negative association between precipitation
and Alternaria spore concentration, precipitation was
significantly and positively associated with Alternaria and
Cladosporium spore levels in the present study. Similarly to
our results, Hjelmroos (1993) reported that dry spore concen-
trations increase at the onset of rain. This phenomenon should
be explained by the fact that dry spores are released from the
sporangium via splash-induced emission (Troutt and Levetin
2001) that releases spores by mechanical shock and fast air
currents produced by raindrops (Elbert et al. 2007). Moreover,
higher concentrations of conidiospores occur in seasons with
higher precipitation and temperatures as was recorded in
Bratislava during the study period (the annual precipitation
total and mean annual air temperature was 133 mm and 0.4
°C higher, respectively than the long-term average) and abun-
dant dead plant material for the fungi to grow on.
It seems that air temperature and daytime period are the
main environmental factors that affect airborne spore concen-
trations of Basidiomycetes. Negative correlations with air
temperature and daytime period appeared in taxa with night-
time highest spore concentrations, as in Agrocybe,
Ganoderma and Coprinus. The negative association between
basidiospore concentrations and air temperature suggested
that spore production or fungal growth is decreased in higher
temperatures.
We also observed a negative relationship between wind
speed and spore concentrations of Coprinus and Ganoderma,
similar to that found in previous studies (Martínez Blanco et al.
2016; Grinn-Gofrońet al. 2018). Large concentrations of
Coprinus and Ganoderma spores were associated with the
bihourly mean wind speed of 2 to 3 m/s (Fig. 2). This is in
accordance with Calderon et al. (1995), who pointed out that
wind speed > 5 m/s is associated with decreased concentrations
of basidiospores, perhaps due to the diluting effect of high wind
velocities on airborne spore concentrations. Moreover, increas-
ing wind speed may inhibit wet spore production due to the
increase in water loss (Calderon et al. 1995). The availability of
atmospheric moisture is necessary to the spore production and
liberation of Basidiomycetes (Hernández Trejo et al. 2013).
However, neither precipitation nor relative air humidity was
significantly associated with spore concentration of any type
of basidiospores in the present study. This could be explained
by a time lag between the spore release and trapping.
Basidiomycetes release spores in moist conditions, however
leading to elevated spore levels several hours after rain (Packe
and Ayres 1985).
Unlike basidiospores, we observed precipitation and rela-
tive air humidity to be significantly associated with
Leptosphaeria ascospore concentration. The association be-
tween precipitation and spore concentrationof mentioned tax-
on was negative, whereas the association between relative air
humidity and spore concentration was positive. Similarly to
our results, research conducted in Taiwan (Kallawicha et al.
2017) has reported a positive association between relative air
humidity and ascospores. The positive influence of relative air
humidity on Leptosphaeria spore levels in the air could be
explained by the fact that many Ascomycetes ascospores re-
quire moisture for their release (Díez Herrero et al. 2006). The
active release of ascospores islikely to occur some period after
the start of precipitation, unlike the ejection of inertly released
conidiospores by droplets which occurs at the commencement
of heavy precipitation. The rain, in small amounts, could be a
stimulating factor for sporulation and spores concentration;
however, when the intensity of precipitation increases, it
operates by removing spores from the atmosphere by both
rain-out and wash-out effects (Sakiyan and Inceoğlu 2003).
Atmospheric pollutants considered in the present study
were also associated with fungal spore concentrations. With
exception of Coprinus and Leptosphaeria,PM
10
exhibited a
positive association with all analysed spore types in the pres-
ent study, which is similar to the results that were reported in
Taipei and Hualien (Taiwan) (Kallawicha et al. 2017;Hoetal.
2005). This could be attributed to the ability of fungal spores
to be adsorbed on the surface of the particulate matter, altering
the particle aerodynamic properties, and thus be dispersed in
the atmosphere (Burge and Rogers 2000). Contrary to our
results, Lin and Li (2000) pointed out that PM
10
did not cor-
relate well with bioaerosols because of the low contribution of
the bioaerosols to the particulate matter.
The tropospheric ozone is a photochemical reaction prod-
uct and the increased solar radiation has a key role in its con-
centration. Therefore, the intradiurnal variations of O
3
concen-
tration showed differences throughout the 24-h period, with a
clear increase in ozone concentrations over the warmer and
dryer parts of the days (Figs. 2and 3). Tropospheric ozone is a
strongly phytotoxic oxidant (Tiedemann and Firsching 2000),
which can suppress the growth of fungi and thus reduce spore
concentration in the air (Sommer et al. 1981). In our multivar-
iate analysis, ozone exhibited significant and negative
associations with Coprinus,Ganoderma and Leptosphaeria
spore types. Similarly to our results, Ho et al. (2005)have
reported negative association between ozone and
Ganoderma spore concentrations.
Environ Sci Pollut Res
In Bratislava, the high concentration of CO and NO
2
in the
air is attributed to increased CO and NO
2
emission from cars
during both the morning and evening traffic peaks between
06:0008:00 and 16:0018:00, respectively (Fig. 3). CO can
suppress the growth of fungi in the environment (Sommer
et al. 1981). However, on the basis of the our study results,
it seems that CO does not influence most of the airborne spore
concentrations as the significant association was only ob-
served with two spore types; the association with Coprinus
was positive, whereas the association with Cladosporium was
negative. Concerning the NO
2
, the spore concentrations of
Agrocybe,Ganoderma and Cladosporium have been ob-
served to increase with increasing atmospheric NO
2
levels,
while the association with Leptosphaeria was negative.
However, more studies are needed to understand the mecha-
nisms of these associations.
Although the proportion of explained variance (Table 2)of
some spore type models were not optimal (R
2
< 0.4), they are
comparable to those in other studies, in which the R
2
ranged
from 0.01 to 0.77 (Troutt and Levetin 2001;Hoetal.2005;
Sousa et al. 2008). Except for meteorological parameters and
air pollutants, the occurrence of those spore types which
showed worse R
2
values can be associated to other environ-
mental factors, such as availability of organic matter for the
development of the fungus. Similarly to Sousa et al. (2010),
Ganoderma and Alternaria presented the best R
2
values in the
present study.
Conclusion
Intradiurnal periodicity of spore concentrations was different
for dry and wet fungal spores. Dry spores (Alternaria,
Cladosporium,Epicoccum,Exosporium) showed a daytime
pattern of the release and subsequently higher concentrations
during the forenoon, noon or afternoon hours, whereas wet
spores (Agrocybe,Coprinus,Ganoderma,Leptosphaeria)
showed a nocturnal pattern of the highest number of spores
during the night or early morning hours.
Results of multiple regression analysis showed that there
was no single model for all spore types. Different combina-
tions of factors were predictors of spore concentration for the
various examined fungal organisms; however, air tempera-
ture, PM
10,
wind speed and precipitation seemed to be the
most important for daytime spore types, while for nighttime
spores, air temperature, daytime interval and O
3
concentra-
tions were identified as the most influential. Except for O
3
and daytime period, all analysed environmental parameters
were positively associated with the concentration of some
daytime spore types, while the association with relative air
humidity and CO was negative. For some nighttime spores,
the association between their spore concentrations and the
following environmental parameters: air temperature,
sunshine duration, wind speed, precipitation, daytime period
and O
3
was negative, whereas the association with relative air
humidity and CO was positive. Some air pollution parameters,
such as PM
10
and NO
2
, had mixed effects on nighttime spore
concentrations, and thus, further research should be made to
examine their health effects.
In general, air temperature, PM
10
and wind speed were
environmental parameters with a great influence, being pres-
ent in eight, seven and four regression models, respectively.
Nevertheless, atmospheric pressure, CO and relative air hu-
midity present almost no influence on the airborne spore
levels.
Acknowledgments The authors would like to thank the Division of
Meteorology and Climatology (Faculty of Mathematics, Physics and
Informatics of Comenius University in Bratislava) for providing meteo-
rological data for Bratislava.
Funding information This study was supported by the Grant Agency
VEGA (Bratislava), Grant Nos. 1/0056/20, 2/0054/18 and 1/0341/19.
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Environ Sci Pollut Res
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... Long-range dispersal of airborne spores over thousands of kilometers is known to occur in nature (Levetin et al. 2015). The production, release and dispersion of spores in the atmosphere are determined by the complex interaction between biological and environmental factors such as: geographical location, air pollution, weather conditions, human activity and local source of vegetation (Grinn-Gofroń and Bosiacka 2015;Š čevková et al. 2019). But in addition to the spores, fragments of the mycelium, fractured conidiophores or other mycelial structures can also be dispersed through the air (Green et al. 2006). ...
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Purpose: Fungi have been known to be important aeroallergens for hundreds of years. Most studies have focused on total fungal concentration; however, the concentration of specific allergenic fungi may be more important on an individual basis. Methods: Ten fungal allergic patients and 2 non-fungal allergic patients were enrolled. The patients with a decrease in physician or patient global assessment by more than 50% of their personal best were considered to have an exacerbation of allergic symptoms and to be in the active stage. Those who maintained their physician and patient global assessment scores at their personal best for more than 3 months were considered to be in the inactive stage. The concentrations of dominant fungi in the patients' houses and outdoors were measured by direct and viable counts at active and inactive stages. Results: The exacerbation of allergic symptoms was not correlated with total fungal spore concentration or the indoor/outdoor ratio (I/O). Specific fungi, such as Cladosporium oxysporum (C. oxyspurum), C. cladosporioides, and Aspergillus niger (A. niger), were found to be significantly higher concentrations in the active stage than in the inactive stage. Presumed allergenic spore concentration threshold levels were 100 CFU/m³ for C. oxysporum, and 10 CFU/m³ for A. niger, Penicillium brevicompactum and Penicillium oxalicum. Conclusions: The major factor causing exacerbation of allergic symptoms in established fungal allergic patients may be the spore concentration of specific allergenic fungi rather than the total fungal concentration. These results may be useful in making recommendations as regards environmental control for fungal allergic patients.
Chapter
Before dealing with the specific problems of aerobiological monitoring, it is necessary to explain how the biological component of air may be a potential cause of degradation in cultural artefacts.