Aerobiologia
https://doi.org/10.1007/s10453-023-09788-5
ORIGINAL PAPER
Manual and automatic quantification of airborne fungal
spores during wheat harvest period
Isidora Simović · Predrag Matavulj ·
Branko Šikoparija
Received: 29 August 2022 / Accepted: 29 March 2023
© The Author(s), under exclusive licence to Springer Nature B.V. 2023
Abstract  Due to the large diversity and quantity
of fungal spores, such aerobiological studies are not
so abundant and haven’t been done in Serbia so far.
As the Pannonian plain is listed as a source of fungal
spores all around Europe, our study aimed to describe
the aerobiological characteristics of airborne fungal
spores measured in location representative for the
Pannonian plain during the wheat harvest period and
to evaluate automatic bioaerosol monitoring for quan-
tification of total airborne fungal spores. The study
revealed that Cladosporium, Alternaria, and Copri-
nus accounted for over 90% of the total fungal spores
count. The relation to meteorology confirmed a dis-
tinction between “dry” and “wet” spores and their
diurnal cycles, as Ganoderma and Coprinus peaked
around dawn, and Alternaria and Cladosporium
peaks correlated with daily peaks of temperature and
relative humidity. Automatically quantified daily con-
centrations of total airborne fungal spores showed a
statistically significant positive correlation (Pearson
r = 0.55, p < 0.01) to values obtained from the manual
Hirst method. The same correlations were found for
Supplementary Information  The online version
contains supplementary material available at https://​doi.​
org/​10.​1007/​s10453-​023-​09788-5.
I. Simović (*) · P. Matavulj · B. Šikoparija  be neglected. There is evidence that 10–48% of sensi-
BioSense Institute ‑ Research Institute for Information
Technologies in Biosystems, University of Novi Sad, Dr
Zorana Djindjica 1, 21000 Novi Sad, Serbia
e-mail: isidora.simovic@biosense.rs
total pollen (Pearson r = 0.60, p < 0.01) and starch
granules (Spearman r = 0.80, p < 0.01). A low inten-
sity of fluorescence measurements for fungal spores
requires a separate automatic detection from pollen
and indicates the need for a good quality training
dataset. Thus, Hirst-type measurements provide an
essential model for classifying bioaerosols with arti-
ficial intelligence.
Keywords  Bioaerosols · Daily cycle · Airflow
cytometer · Laser induced fluorescence
1 Introduction
Airborne fungal spores constitute an important pro-
portion of atmospheric particles of biological ori-
gin (Adhikari et  al., 2004; Ataygul et  al., 2007) and
some are recognized as being linked with detrimental
effects on human health (Horner et al., 1995; Lacey,
1997). Studies have demonstrated significant asso-
ciations between Alternaria and Cladosporium with
asthma in susceptible atopic patients (Horner et  al.,
1995, Ostro et al. 2001, Douwes et al., 2003). Despite
these two constituting up to 93% of the total fungal
spores in a study that covered 10 fungal taxa found in
the air (Ataygul et al., 2007), other spores should not
tization in skin prick tests of the atopic population has
been attributed to Ganoderma spores (Butcher et al.,
1987; Singh et al., 1995; Tarlo et al., 1979) which can
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 Aerobiologia
also induce an allergenic response in sensitized indi-
viduals (Vijay et  al., 1991). Ganoderma is cited to
cause reactions in nearly 30% of patients with asthma
(Cutten et al., 1988) and similarly, patients with aller-
gic or non-allergic rhinitis reacted to Ganoderma in
the study of Rivera-Mariani et al., 2011. Tham et al.,
2017 found weak associations between some taxa,
Ganoderma among others, to the children and adoles-
cents who were hospitalized for asthma in Australia.
Some species of Epicoccum produce highly allergenic
spores that can trigger high cutaneous reactivities,
sharing allergenicity with different fungi responsible
for the allergic type I symptomatology (Bisht et  al.,
2004). For the Drechslera type strong positive reac-
tions have been documented in cutaneous testes in
atopic individuals (Kasprzyk et  al., 2021) and its
abundance in the atmosphere has been significantly
associated with asthma hospitalizations (Tham et al.,
2017).
Many fungal spores have been shown to have
implications for agricultural and forest ecosystems.
Ganoderma is an important plant pathogen that
attacks healthy forest ecosystems listed as a com-
mon cause of disorder in several species in healthy
forests (McKay, 2011) by causing white rot of trees
(Blanchette, 1984) and Alternaria causes early blight
in potatoes (Harrison et al., 1965). Up to almost 60%
of agricultural yield losses caused by Alternaria spe-
cies were registered in the study of Singh et al., 2014.
Alternaria and Drecshlera are common and wide-
spread pathogens in wheat (Li and Yoshizawa, 2000).
The data on airborne fungal spores are rare in
comparison to pollen data (Skjøth et al., 2012). Since
the start of using the Volumetric Hirst method in aer-
obiological studies in Serbia, the focus was mainly
on pollen grains relevant to allergology (Radišić &
Sikoparija, 2005; Sikoparija et al., 2006) and agricul-
ture (Prentovic et  al. 2014). Only recently, after the
successful participation in fungal spores identification
quality control organized by EAS (Galán et al., 2021),
the conditions to study airborne fungal spores were
met. Due to time-consuming and labor-demanding
traditional methods of fungal spores concentration
count as well as difficulties associated with the identi-
fication, diurnal profiles of major fungal spores types
in Serbia have not been established so far.
With the efforts to establish automatic quan-
tification of airborne pollen (Smith et  al., 2022;
Tešendić et  al., 2020), knowledge of the diversity
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of other bioaerosols became essential for develop-
ing classification models and for interpreting their
performance. In addition, the annual peak concen-
trations of airborne fungal spores have been shown
to be related to specific agricultural operations such
as harvesting of crops (Friesen et  al., 2001; Skjøth
et al., 2012) making Pannonian plain, a dominantly
agricultural region, an important source of spores
not only locally but around Europe (Grewling
et al., 2022). There were several recent studies that
described the performance of automatic systems in
quantifying airborne fungal spores. Automatization
of classifications of Alternaria from classic micros-
copy images yielded good performance (Wu et  al.,
2018) because of very distinctive morphology. Both
using classic microscopy images from impactor
(González-Alonso et  al., 2023) and airflow cytom-
etry with holograms (Erb et al., 2023) yielded good
results when compared to manual measurements
from Hirst-type volumetric approach.
The aim of this study was to describe the aerobi-
ological characteristics of pollen and fungal spores
detected during the month of wheat harvest in the
Pannonian plain and to explore the possibility to
discriminate and quantify bioaerosols from a signal
obtained by the airflow cytometer Rapid-E (Plair
SA).
2 Material and methods
2.1 Study area
Continuous aerobiological sampling was performed
at roof level (20 m a.g.l.) in Novi Sad (45.245575°
N, 19.853453° E) both by a manual sampler of the
Hirst design (1952) and by the automatic bioaerosol
monitor (Šaulienė et  al., 2019). The aerobiological
measurements were situated in Autonomous Prov-
ince Vojvodina and thus are deemed representative
of the Southern Pannonian plain, which is a flat area
predominantly occupied by agriculture, in particu-
lar, arable crops (Lugonja et al., 2019).
Since it is expected that the wheat harvest gen-
erates large emissions of airborne fungal spores
(Skjøth et al., 2012), the analysis focused on meas-
urements during July 2019.
Aerobiologia
2.2 Aerobiology data
2.2.1 Manual Hirst type measurements
Airborne pollen and fungal spores were sampled by
Lanzoni VPPS2000 volumetric pollen and spores trap
of the Hirst (1952) design that continuously sucked
10 l ­min−1 through a 2 mm × 14 mm orifice oriented
towards the direction of the wind. Particles carried
by the airflow are impacted onto an adhesive-coated,
transparent plastic tape that moves behind the orifice
at 2  mm/h. Following its removal from the trap, the
segments of the tape corresponding to 24-h periods
(48  mm in length) were mounted on a microscope
slide and analyzed by a light microscope at × 400
magnification. Fungal spores were recorded at each
4  mm segment of the tape (corresponding to 2  h of
the sample) along one horizontal transect (i.e. 3.86%
of the sample). Ten distinctive taxa were recorded
(Alternaria, Cladosporium, Coprinus, Drechslera,
Epicoccum, Ganoderma, Myxomycetae, Periconia,
Peronospora, urediniospores), and all the rest were
classified either as hyaline if transparent or unknown.
In order to be aligned with automatic bioaerosols
detections fungal spores larger than about 8 microns
were counted separately. In addition to fungal spores,
pollen grains, and starch particles were recorded.
Although the analyzed surface is smaller than recom-
mended by the standard method EN16868:2019 (EN,
16868, 2019) and the minimum requirements for
pollen monitoring described by Galán et  al. (2014),
a large quantity of detected particles decreases the
uncertainty from the subsampling. The results were
presented as pollen concentrations (pollen ­ m−3),
−3
fungal spores concentration (spores ­m ), and starch
granules concentrations (starch m ­ −3) (Galán et  al.,
2017), determined by the rotation speed of the drum,
the width of the sampling orifice and volume of sam-
pled air. Both 2-h concentrations and daily averages
were analysed.
2.2.2 Automatic bioaerosol measurements
Automatic bioaerosol measurements were performed
using the Plair SA Rapid-E, which continuously sam-
ples about 2.8  l  ­min−1 of air and measures the scat-
tered light and fluorescence of each particle (Šaulienė
et al., 2019). The Rapid-E was operated in the “smart
pollen mode” (Šikoparija, 2020) in which parti-
cles < 8 μm in optical diameter are filtered out.
The collected signal is expected to provide infor-
mation about the morphology and chemical compo-
sition of each detected particle (Kiselev et al., 2011,
2013), and as such is expected to allow identifica-
tion. Since laser-induced fluorescence data tend to be
noisy, we have filtered out measurements with insuf-
ficient fluorescence intensity (i.e. the maximum spec-
trum intensity less than 2500). Also, measurements
where four maxima of the spectrum are not between
400 and 500  nm, as expected in common bioaero-
sols after the excitation with near-ultraviolet laser
(O’Connor et  al., 2011; Pöhlker et  al., 2012) were
excluded from the analysis. The classification model
is based on convolutional neural networks (CNN)
(Tešendić et  al., 2020). It extracts features for each
input separately with convolutional blocks consist-
ing of 2D convolutions, ReLU activations, batch nor-
malization, max pooling, and drop out. Features are
then equalized in size with a fully connected layer,
concatenated, and classified with one more fully con-
nected layer and a log-softmax function. The optimi-
zation is performed using the negative log-likelihood
function and the Stochastic Gradient Descent with
a 0.001 learning rate and momentum of 0.9. Since
no reference material for fungal spores was avail-
able the class “total fungal spores” has been created
from particles recorded during periods when large
quantities of fungal spores could be observed in sam-
ples collected using Lanzoni VPPS2000 while very
few other bioaerosols are detected (Supplementary
Fig.  1a, 1b) i.e. 3 June (22:01–23:58UTC), 4 June
(00:01–3:58UTC), 6 June (00:01–1:58UTC), 18 June
(18:01–19:58UTC), 21 June (18:01–19:58UTC), 24
June (22:01–23:58UTC), 26 June (12:01–13:58UTC)
27 June (21:01–21:58UTC) and 28 June
(12:01–13:58UTC). For classifying total fungal
spores, the classification model had to be trained
to discriminate from other abundant bioaero-
sols (Tešendić et  al., 2020). The class “total pol-
len” was created from 13 pollen types commonly
recorded in the atmosphere of the study region in
July i.e., Ambrosia, Artemisia, Cannabis, Carex,
Chenopodium, Humulus, Juncus, Parietaria, Pinus,
Plantago, Poaceae (mix several genera), Tilia,
Urtica. The model was also trained to classify air-
borne starch that is often recorded in the atmos-
phere of the studied region (Šikoparija et  al., 2022)
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 Aerobiologia
by labeling a number of representative particles
from periods when very few other large bioaerosols
were detected i.e., 27 February (16:47–18:15UTC),
20 March (17:01–17:42UTC, 18:01–18:06UTC,
19:01–19:58UTC), 21 March (17:07–17:23UTC) and
23 March (16:37–17:43UTC). In order to limit false
positives from different other particles suspended in
the air, the class “other aerosols” has been created
from particles recorded during periods when no fun-
gal spores, no pollen, or starch are observed in sam-
ples collected using Lanzoni VPPS2000 (Supplemen-
tary Fig.  2c, 2d) i.e., 25 February (7:01–8:58UTC),
25 February (23:01–23:58UTC), 26 February
(00:01–2:58UTC), 13 March (01:01–2:58UTC) and
14 March (18:01–18:58UTC). 90% of samples from
each class were used for the training of the classifica-
tion model while the remaining events were used for
testing.
Detections for 60 min were summed and converted
to hourly concentrations using the 60-min average
flow measurements that the device records in the log
files. In order to be aligned with the manual Hirst-
type measurements, hourly values were averaged to
get 2-h and daily concentrations.
2.3 Meteorology data
Meteorological conditions were recorded with an
automated weather station measuring solar radiation,
air temperature, relative humidity, wind speed, and
precipitation, placed between Lanzoni VPPS2000 and
Plair Rapid-E. The measurements were performed at
1 Hz temporal resolution but to align with the resolu-
tion of the Hirst-type trap, meteorological data were
averaged to 2-h and 24-h resolution.
2.4 Data analysis
The aerobiological characteristics of airborne fungal
spores detected in Novi Sad during July 2019 have
been described by Monthly Pollen Integral (MPIn)
expressed as pollen * day m ­ −3 and Monthly Spore
Integral (MSIn) expressed as spores * day ­m−3, maxi-
mum concentration, and % of days when pollen and
spores were detected.
Daily average and 2-hourly spores concentra-
tions collected by standard EN16868 and automatic
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method and meteorological data were examined for
normality using the Shapiro–Wilk test. Correlation
analysis was then used to determine whether fungal
spores’ concentrations are related to meteorologi-
cal conditions and also applied to determine whether
detections by Hirst-type and Rapid-E devices were
significantly related. Pearson correlation coefficients
were applied when data were normally distributed
otherwise Spearman correlation coefficients were
calculated.
3 Results
3.1 Airborne pollen and fungal spores
Standard bioaerosol measurements in Novi Sad dur-
ing July 2019 revealed notable dominance of fun-
gal spores in the atmosphere. Total pollen integral
of 3697 Pollen * day ­m−3 and 24 pollen types with
Urticaceae being the most abundant, followed by
Poaceae, Plantago, and Cannabaceae has been meas-
ured (Table  1). On the other hand, the total fungal
spores integral of 311,562 Spores * day m ­ −3 is meas-
ured. The most abundant spores are Cladosporium,
followed by Coprinus, Alternaria, various hyaline
spores, and Ganoderma (Table 1). Hyphal fragments
constituted a significant part of the Novi Sad atmos-
phere, being more frequent than the rest of the fun-
gal spores. Cladosporium, Alternaria, Epiccocum,
and fragmented hyphae are recorded during the entire
period showing short-term fluctuations in quantity
(Fig.  1). While Coprinus spores are the most abun-
dant in mid-July, the Urediniospores are more abun-
dant in the beginning and at the end of the month.
Drechslera and Myxomycetes are more abundant in
the first half of the month while Ganoderma, Perico-
nia, and Peronospora are more abundant in the sec-
ond half of the month. Hyaline spores are abundant
until mid-July and then after a discernible decline,
there is a clear peak in the last four days of July.
During day hours (in particular, in the afternoon)
the following fungal spores are recorded: Alternaria,
Cladosporium, Drechslera, Epiccocum, hyphae, Per-
onospora, and uredinospores. On the other hand,
most of Coprinus, Ganoderma, and hyaline spores are
recorded during night hours (Supplementary Fig. 2).
Aerobiologia

Table 1  The list of detected pollen types and fungal spores in Novi Sad during June 2019
Class MPIn [pollen * day ­m−3] (% of Maximum daily concentration [pollen % of days recorded
the total) ­m−3]

Pollen grains
 Alnus 1 (0.03%) 1 3
 Ambrosia 62 (1.7%) 17 45
 Apiaceae 9 (0.2%) 1 29
 Artemisia 69 (1.9%) 13 52
 Asteraceae 34 (0.9%) 16 48
 Cannabaceae 135 (3.7%) 25 68
 Castanea 2 (0.1%) 1 6
 Chenopodiaceae 65 (1.8%) 8 87
 Cyperaceae 1 (0.03%) 1 3
 Hedera 2 (0.1%) 2 3
 Iva 3 (0.1%) 1 10
 Pinaceae 11 (0.3%) 2 32
 Plantago 229 (6.2%) 24 100
 Platanus 1 (0.03%) 1 3
 Poaceae 269 (7.3%) 18 100
 Rubiaceae 6 (0.2%) 1 19
 Rumex 5 (0.1%) 1 16
 Sophora 1 (0.03%) 1 3
 Cichoriaceae 4 (0.1%) 1 13
 Cupressales 4 (0.1%) 2 10
 Tilia 45 (1.2%) 16 68
 Typha 3 (0.1%) 2 6
 Urticaceae 2734 (74%) 338 100
 Xanthium 2 (0.1%) 1 6
 TOTAL 3697 400
Fungal spoRES
 Alternaria 18,614 (6%) 1366 100
 Cladosporium 218,849 (70.2%) 25,542 100
 Coprinus 26,599 (8.5%) 2549 100
 Drechslera 686 (0.2%) 175 100
 Epicoccum 3141 (1%) 338 100
 Ganoderma 7133 (2.3%) 796 100
 hyphae 8539 (2.7%) 704 100
 hyaline 11,639 (3.7%) 1361 100
 Myxomycetae 256 (0.1%) 38 71
 Periconia 295 (0.1%) 36 65
 Peronospora 641 (0.2%) 88 94
 urediniospores 679 (0.2%) 49 100
 unknown 14,492 (4.7%) 1566 100
 TOTAL 311,562 28,728

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 Aerobiologia
◂Fig. 1  Daily concentrations of airborne fungal spores meas-
ured in Novi Sad in July 2019 a Alternaria, b Cladosporium, c
Coprinus, d Drechslera, e Epiccocum, f Ganoderma, g hyphae,
h hyaline, i Myxomicetae, j Periconia, k Peronospora, l uredi-
nospores. (y-axes have different scale)
In addition to pollen and fungal spores, the sam-
ples contained a notable amount of starch granules
(MPIn 7576 Starch * day ­m−3). There were six dis-
tinctive episodes during which 2-h concentrations of
starch granules larger than about 8 microns exceeded
1000 Starch m­ −3.
3.2 Relation to meteorological conditions
Observed patterns in the occurrence of different
spores along the study period imply the impor-
tance of meteorological parameters, both during the
month and diurnal cycles. Temperature, humidity,
and solar radiation followed the normal daily cycle
(Supplementary Fig. 3). On average the study period
is characterized by the mean daily temperature
of 23.7  °C, mean daily relative humidity of 59.1%
mean daily solar radiation of 254.1  h, and the sum
of precipitations of 23.1  mm. The air temperature
was somewhat higher at the beginning of the month
and in the period between 21st July and 27th July.
Relative humidity exceeded 70% only in mid-July
and precipitations were registered during only seven
days in July. Solar radiation was 250-300  h and
dropped below 150 h only around days with precipi-
tation. The most frequent wind was from a South-
Westerly direction.
Daily concentrations of Alternaria spores are sig-
nificantly negatively correlated with humidity and
rainfall while positively correlated to solar radiation
(Supplementary Table  1). Surprisingly, the relation
to temperature was not significant. On the other hand,
hyaline spores are positively correlated to humidity
and rainfall and negatively correlated to radiation.
Interestingly, only Ganoderma showed a significant
correlation to temperatures. Coprinus spores did not
correlate to any of the meteorological parameters
although the highest concentrations were detected
on the 7th of July and 29th of July when the heavi-
est rainfall was registered. There was, however, some
congruence of high spores count to the wind of the
SW direction.
It is interesting to note that when looking at
the diurnal resolution, Spearman’s rank test (Sup-
plementary Table  2) indicates relationships with
meteorology that correspond to night-day changes.
Ganoderma, Coprinus, and hyaline spores are nega-
tively correlated to temperature and radiation but are
strongly positively correlated to humidity which is
in line with their more frequent night records (Sup-
plementary Fig. 2c and 2f). On the other hand, most
other spores that correlate positively with tempera-
ture and radiation while being negatively correlated
to humidity, are in line with their more frequent day-
time records.
3.3 Automatic measurements
The integral of particles recorded by the Rapid-E
device running in “smartpollen” mode was 574,360
Particles * day ­m−3 while only 23,698 Particles *
day ­m−3 remained after filtering out those that were
considered of insufficient quality. 2-hourly total par-
ticle count did not show a statistically significant
correlation between total fungal spores (Spearman’s
Rho = 0.13, p = 0.50) measured side-by-side using
Hirst volumetric standard method.
In the CNN classification model, the average F1
score on the test dataset was 78.26% but the spores
were classified with limited accuracy (50%) with
“other aerosols” being notably misclassified as fun-
gal spores (Supplementary Fig. 4). Automatic detec-
tion of total pollen, and total fungal spores, recorded
fewer particles than is measured by the standard
method (EN16868) but the correlations to side-by-
side measurements using Hirst volumetric standard
method were statistically significant, for both, for
2-hourly and daily temporal resolution (Table  2).
Despite the expected uncertainty of 2-hourly data,
the automatic detection of total pollen, total fun-
gal spores, and starch granules clearly indicate an
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Table 2  Monthly Integrals (MIn) and scaling for total pollen
(sum of classified pollen types), total fungal spores and starch
granules larger than about 8 microns correlations between con-
Class Hirst MIn Rapid-E MIn
Total pollen 4528 2250
Total fungal spores 89,410 3077
Starch granules 7576 1201
All correlations are statistically significant at p < 0.01
a
 Pearson
b
 Spearman
increase and decrease in concentrations as seen by the
standard Hirst volumetric measurements (Supplemen-
tary Fig. 5). For starch granules, automatic detections
have a great number of false positives but the distinc-
tive peaks are clearly visible.
4 Discussion
July is generally characterized by the largest diver-
sity and quantity of airborne fungal spores in our cli-
mate zone (Ščevková & Kováč, 2019) and this goes
for urban parks as well (Kasprzyk et al., 2021). It is
important to emphasize that, in this study, reported
fungi are just a fraction of full diversity. Hyaline
spores and unknown class contain a large spectrum
of taxa which, to be revealed, require more specific,
eDNA methods like those proposed by Nicolaisen
et al. (2017). The diversity of fungal spores recorded
in July in Novi Sad includes both, known allergenic
spores and those that are recognized plant pathogens
(Magyar et  al., 2009; Van der Heyden et  al., 2021).
Similar to the findings from South America (Hen-
ríquez et  al., 2001), North America (Gillum & Lev-
etin, 2008), Australia (Mitakakis & Guest, 2001),
Asia (Ho et  al., 2005; Hasnain et  al., 2012; Hasnain
et  al., 2005) and throughout Europe (Myszkowska
et al., 2002; Pepeljnjak & Šegvić, 2003; Damialis &
Gioulekas, 2006; Herrero et  al., 2006; Vélez-Pereira
et  al., 2016; Jesús Aira et  al., 2012; Oliveira et  al.,
2009; Sousa et al., 2016), Cladosporium is the main
component of airborne mycobiota in the Pannonian
plain with concentrations comparable to the areas
considered as the most polluted with airborne fungal
spores in Europe (Spieksma, 1995). It is followed by
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centrations (daily and 2-hourly) measured following manual
EN16868 method and CNN classification from Rapid-E device
Scaling [Hirst/ Correlation coefficient
Rapid-E]
Daily 2-hourly
2.01 0.60a 0.57b
29.06 0.55a 0.46b
6.31 0.80b 0.32b
Alternaria, Coprinus, and the diverse group of hya-
line spores. The abundance of hyphal fragments was
cited by previous researchers as well (Akgül et  al.,
2016) where its concentrations even surpassed Alter-
natia unlike in our study.
The analysis of meteorological conditions con-
firmed the ‘dry’ spores character for Cladosporium,
Alternaria, Epicoccum, and Dreschlera spores (Burch
& Levetin, 2002; Ianovici, 2016; Troutt & Levetin,
2001), while Coprinus and hyaline spores are related
to ‘wet’ conditions (Antón et  al., 2019). Although
the dataset is limited to just one month, analysis of
diurnal patterns with clear day-night differences
confirmed preferences for humidity and moisture by
predominance in night hours records for Ganoderma
(Craig & Levetin, 2000; O’Connor et  al., 2014) and
Coprinus (Aira et  al., 2009; Almaguer et  al., 2014).
Diurnal patterns of fungal spores such as Clad-
osporium and Coprinus have been described before
by Burge, 1986. Skjøth et al. (2016) found that local
climate, vegetation patterns, and management of the
landscape are governing parameters for the overall
concentration of airborne spores, while the annual
variations caused by weather are of secondary impor-
tance. The most abundant spores in the atmosphere
grow on vegetation (Grinn-Gofroń et  al., 2020) thus
predominant agricultural land use in the study area
with arable crops (Lugonja et  al., 2019) explains
large concentrations of Cladosporium and Alter-
naria spores detected in this study. On the other hand,
Coprinus high concentrations are related to orchards
(Russo et  al., 2015; Grinn-Gofroń et  al., 2020) but
urban sources should not be neglected (Kokkoris
et  al., 2019) and so as the vicinity of Fruska Gora
Aerobiologia
mountain with notable populations of Ganoderma
(Karaman & Matavuly, 2005).
The artificial intelligence-based model for the
classification of bioaerosols gave results that cor-
related positively to standard Hirst-type volumet-
ric measurements both for total pollen and starch
concentrations. The intensity of correlation for
starch granules was about 10% lower than what
was seen when the entire season has been analyzed
(Šikoparija et  al., 2022). This is attributed to the
short analysis period which had only six notable
episodes with an abundance of starch granules. An
even more notable decrease in correlation intensity
has been seen for total pollen when compared to the
full season (Smith et  al., 2022). This can also be
attributed to the shorter analysis period and the fact
that July is considered a low pollen season in AP
Vojvodina (Smith et  al., 2022) which emphasizes
the uncertainty of the standard method (EN16868).
The uncertainty in our study is additionally aug-
mented by analyzing less than 10% of the sample.
Therefore, analysis of finer temporal resolution
should be taken with caution. Also, it should be
noted that the scaling of the Rapid-E signal was
linear in our study, and since it was shown that the
scaling is pollen type-specific (Smith et  al., 2022)
it could be expected that alignment with Hirst-type
data could be further improved if the scaling is done
separately for each classified pollen type before
aggregating into total pollen class. However, even
the correlation coefficient exceeded the values for
Rapid-E seen in recent tests of several operational
airflow cytometers (Tummon et al., 2021).
Our study confirmed that regular measurements
could be used for creating training datasets for
developing models for classifying bioaerosols of
interest. This approach is particularly useful when
it is difficult to collect reference material such as in
the case of fungal spores (i.e., unknown medium for
successful sporulation and problems with aerosoli-
zation because of either difficulty in detaching from
the colony or excessive clustering of particles). A
similar approach has successfully been applied in
the model that classifies Alternaria airborne spores
(Erb et al., 2023). However, the quality of the classi-
fication model depends on the cleanness of the train-
ing dataset which makes the image airflow cytometer
(Sauvageat et al., 2020) more suitable in comparison
to other operational airflow cytometers (Lieberherr
et al., 2021). The exception to this is when the par-
ticle of interest during the selected period can effi-
ciently be distinguished from others by, for exam-
ple, the size of the fluorescence character. Also, for
training a robust classification model large number
of reference particles is needed. It could be difficult
to find suitable periods in routine measurements in
which the desired particle is recorded in large quan-
tities and, at the same time, dominates among other
aerosols.
It is important to note here that despite the posi-
tive correlation between standard and automatic
measurements, there is often a need for scaling
(Tešendić et al., 2020; González-Alonso et al., 2023)
which appears to be specific to the class of interest
(Smith et al., 2022). The size of scaling is related to
losses from filtering out particles with lower quality
signals which in our study were more than 10 times
for fungal spores than pollen, probably because of
overall lower intensity fluorescence measurements
(O’Connor et  al., 2011). To overcome this problem
the gain of the detectors should be increased but that
might require measuring separately weak fluoresc-
ing particles and pollen to avoid saturation of the
signal.
5 Conclusion
The analysis of aerobiological data from the stud-
ied region confirmed the importance of meteorol-
ogy and potential surrounding sources for the char-
acteristics of airborne fungal spores. As expected,
concentrations of airborne fungal spores notably
exceed the quantity of airborne pollen in the study
period. Unlike starch granules, airborne fungal
spores were continuously present in the atmos-
phere, which emphasizes the importance of con-
tinuous monitoring. Airflow cytometry measuring
scattering and laser-induced fluorescence from
particles suspended in the air when coupled with
artificial intelligence enables automatic detection
of total fungal spores. Good reference dataset for
training classification model remains challenging.
Until a standard collection of fungal spores domi-
nant in the atmosphere is available, using specific
episodes from real-life measurements will enable
the detection of groups of fungal spores. In this
approach, more specific detections are possible,
Vol.: (0123456789)
13
 Aerobiologia
if such episodes consist of a single spores type
(which is very rare) or if there is a suitable method
for cleaning the dataset from unwanted particles.
Finally, the automatic detection of total fungal
spores required more scaling than is the case for
pollen. Low intensity of fungal spores fluores-
cence resulted in more particles filtered out by
fluorescence threshold. Therefore, more sensitive
detectors are required but to avoid saturation of
signal from intensively fluorescing particles (such
are pollen grains) the measurements should be
conducted separately (i.e., by changing the gain of
detectors consecutively in regular intervals).
Author contribution  Isidora Simovic: Investigation, Formal
analysis, Data curation, Writing—original draft; Predrag Mata-
vulj: Formal analysis; Branko Sikoparija: Conceptualization,
Formal analysis, Writing – original draft, reviewing and edit-
ing, Funding acquisition.
Funding This research was partially funded by the
BREATHE project from the Science Fund of the Republic of
Serbia PROMIS program, under Grant agreement no. 6039613
and by the Ministry of Education, Science and Technologi-
cal Development of the Republic of Serbia (Grant agreement
numbers 451-03-68/2022-14/200358). Measurement campaign
in Novi Sad was supported by RealForAll project (2017HR-
RS151) co-financed by the Interreg IPA Cross-border Coopera-
tion program Croatia—Serbia 2014–2020 and Provincial secre-
tariat for finances, Autonomous Province Vojvodina, Republic
of Serbia (contract no. 102-401-337/2017-02-4-35-8).
Data availability  The data that support the findings of this
study are available upon reasonable request from the authors.
Declarations 
Conflict of interest  The authors declare that they have no
known competing financial interests or personal relationships
that could have appeared to influence the work reported in this
paper.
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