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ORIGINAL PAPER
Diversity and annual fluctuations of culturable airborne
fungi in Athens, Greece: a 4-year study
Ioanna Pyrri •Evangelia Kapsanaki-Gotsi
Received: 11 October 2010 / Accepted: 27 September 2011
ÓSpringer Science+Business Media B.V. 2011
Abstract The diversity and the abundance of the
culturable airborne fungi have been studied by a
volumetric method in the city of Athens, for a period
of 4 years. A total of 6,600 plates were exposed during
562 calendar days, and 70,583 colonies of fungi have
been recovered and studied in detail. One hundred and
forty-eight species in fifty-four genera of filamentous
fungi were identified. A total of three hundred and
twenty strains were isolated and maintained as refer-
ence material. The annual mean concentration of the
total fungi was 538, 640, 694 and 638 CFU/m
3
, and
the concentration range, 25–2,435, 117–2,822,
122–2,201 and 116–2,590 CFU/m
3
for each year,
respectively. There is no statistically significant year-
to-year variation in the distribution patterns and in the
annual mean concentrations of the total fungi. The
diversity and the abundance of the total fungi and of
the dominant genera Cladosporium,Aspergillus and
Alternaria were increased, whereas those of Penicil-
lium decreased during the warm months of each year.
The majority of the species are newly reported as
airborne from Greece. Also, 19 genera and 93 species
are totally new records for this country. The species
Acrodontium virellum,Aspergillus aculeatus,
A. tubingensis,Circinella minor,C. umbellata,
Cladosporium breviramosum,C. malorum,Drechs-
lera tetramera,Paecilomyces crustaceus,Petriella
guttulata,Rutola graminis and Sporotrichum pruino-
sum are reported as airborne for the first time
worldwide.
Keywords Airborne fungi Culture-based
volumetric method Species diversity
Concentration
1 Introduction
Most fungi liberate their spores into the atmosphere
and disseminate them by the air currents. The aerosols
constitute an ephemeral sink of fungal propagules
continuously supplied by the mycobiota. Members of
all the fungal groups in terrestrial habitats, regardless
of their origin, may be found in the bioaerosols during
their dispersal phase. Once the spores become air-
borne, they may colonize new suitable substrates
exposed to the air. As a result, the fungal spores are
ubiquitous, and they mediate numerous processes with
a crucial role in the maintenance and function of any
natural ecosystem. Nevertheless, they may cause
various diseases in cultivated plants in the agroeco-
systems, as well as allergic reactions, infections or
toxicosis to humans. They may also interfere with
several man-made ecosystems and cause deterioration
of materials including foodstuffs, industrial products,
archives and works of art. The knowledge on the
I. Pyrri E. Kapsanaki-Gotsi (&)
Department of Ecology & Systematics, Faculty of
Biology, National and Kapodistrian University of Athens,
Panepistimioupoli, 157 84 Athens, Greece
e-mail: ekapsan@biol.uoa.gr
123
Aerobiologia
DOI 10.1007/s10453-011-9233-z
diversity of the airborne fungi is significant for several
applied issues, with an increased concern for human
and plant health.
Although the common genera of airborne fungi are
adequately known around the world, there is a lack of
information concerning the less frequent and the rare
fungi. Most of the aerobiological surveys record the
fungi at the genus level, and information is missing at
the species level. Moreover, a non-culture-based
sampling method does not allow the identification of
fungi that produce spores not easily recognizable.
Also, the data on the abundance of the fungi are
insufficient in the case of the outdoor airspora studied
by the sedimentation method. A culture-based volu-
metric method records more reliably the diversity of
airborne fungi and their anamorphs, although it fails to
survey thoroughly the total fungi (Pyrri and Kapsa-
naki-Gotsi 2007a). The air mycobiota have been
studied by this method in several countries around
the world (Abdel Hameed et al. 2009; Adhikari et al.
2004; Airaudi and Filipello Marchisio 1996;
Al-Suwaine et al. 1999; Calvo et al. 1980a,b,1981;
Das and Gupta-Bhattacharya 2008; Ebner et al. 1992;
El-Morsy 2006; Fang et al. 2005; Filipello Marchisio
and Airaudi 2001; Filipello Marchisio et al. 1992,
1997; Herrero et al. 1996; Larsen and Gravesen 1991;
O’Gorman and Fuller 2008; Roses-Codinachs et al.
1992; Takahashi 1997; Wu et al. 2007).
In Greece, the published data on the bioaerosols are
mostly concerned with the occurrence and concentra-
tion of certain genera of allergenic fungi studied by
non-culture-based volumetric methods. A detailed
account on the aeromycological studies in Greece has
been presented earlier (Kapsanaki-Gotsi 2007; Pyrri
and Kapsanaki-Gotsi 2007a).
The aim of this paper is to present the diversity and
abundance of the culturable airborne fungi studied by
a volumetric method. It is part of an investigation on
the airborne fungi in the ambient air in the center of
Athens, by ‘‘culture-based’’ and ‘‘non-culture-based’’
sampling methods.
2 Materials and methods
2.1 Sampling site
Athens is a densely populated city within the Attica
basin that is surrounded by mountains and extends to
the sea, along the Saronic Gulf in the southwest. The
whole region has a variable geomorphology, and the
Attica plain is surrounded by the mountain ranges of
Parnitha to the north, Pendeli to the northeast, Ymittos
to the east and Aegaleo to the west. The main rocks are
limestone, marble and schist, which support a rich
flora, including more than 1,000 plant taxa. The upper
zone of Parnitha, which is the highest mountain
(1,413 m) in the region, is dominated by Abies
cephalonica forests. The periurban forests are domi-
nated by Pinus halepensis mixed with Quercus
coccifera, Q. pubescens, Juniperus oxycedrus and
Cupressus sempervirens, in the lowlands intermixed
with Cercis siliquastrum, Olea europaea, Ficus carica
and Prunus spp. The maquis vegetation includes
Pistacia lentiscus, Arbutus unedo, Myrtus communis,
Laurus nobilis, Erica arborea etc. The phryganic
ecosystems consist mainly of Sarcopoterium spino-
sum, Euphorbia acanthothamnos, Corydothymus
capitatus, Phlomis fruticosa, Asphodelus and Cistus
spp. The city has a mild Mediterranean climate with
very hot and dry summers.
The airborne fungi were sampled in the ambient air
in the center of the Athens metropolitan area, which is
occupied by high buildings and has mostly narrow
streets and relatively few patches of vegetation in
public parks. Also, this area is bound by the hills of
Filopappou, Acropolis, Lycabettus and Tourkovounia.
The samplings were made on the rooftop of a building
of the Ministry of the Environment, located at
37°5905800 N, 23°4305900 E, approximately 30 m above
the ground level and 1 m above the floor of the terrace.
The sampling site is in a higher level than the roofs of
the adjacent buildings, situated in a place where the air
currents circulate unobstructed through the Attica
basin.
2.2 Sampling protocol
A portable air sampler for agar plates (Burkard
Manufacturing Company Ltd) with a suction rate of
20 L/min was used for the collection of the air
samples.
Sampling has taken place three times a week, each
Monday, Wednesday and Friday, between 8 and 8:30
a.m. The concentration of the total fungi and the
number of genera recovered are higher in the early
morning, as it was revealed after a diurnal study (Pyrri
Aerobiologia
123
and Kapsanaki-Gotsi 2006). The samplings were
performed all year-round, from January 1998 until
December 2001. A few samplings were omitted for
unforeseen reasons.
Several nutrient media were tested in order to select
the more suitable on the basis of the higher number of
genera recovered in higher concentrations (Pyrri and
Kapsanaki-Gotsi 2007b). The nutrient medium potato
dextrose agar (PDA) was used continuously through-
out the 4 years and additionally malt agar (MA) 2%
the last 3 years. In each sampling date, the sampler
was loaded with twelve plastic Petri dishes of 9 mm
diameter (6PDA ?6MA), which were exposed con-
secutively for 1 min each. The sampler was disinfec-
ted with 70% ethanol before the sampling.
2.3 Isolation and identification of fungi
The exposed plates were incubated at 25°C in the dark
for 7–21 days. Fungal strains that failed to sporulate
after 21 days have been recorded as non-sporulating
fungi (NSF). The colonies were studied for their
macroscopic and microscopic characteristics and
identified at least to the genus level. Representative
strains of the fungi grown in the plates were isolated in
pure culture. The isolated fungal strains in the genera
Penicillium,Aspergillus, Fusarium, Scopulariopsis
and Chaetomium were subcultured in specific nutrient
media and incubated in conditions suitable for each
genus, in order to identify the fungal strains to the
species level. The identification was based on the
detailed study of all the microscopic morphological
characters of the fungi and the macroscopic features of
their colonies. For the resolution of the taxonomic
status of several strains, comparative material from the
ATHUM, BPIC, CBS, CCF, FRR, MUCL, NRRL and
UAMH Collections has been additionally studied.
The isolated fungal strains have been deposited in
the ATHUM Culture Collection of fungi, in the
University of Athens.
2.4 Concentration of fungi in the air samples
The colony counts were corrected by using the
multiple infection transformation factors (Gregory
1948) and were converted to colony-forming units per
cubic meter (CFU/m
3
) of air sampled.
2.5 Statistical analysis
The daily concentrations of the total fungi and the
predominant genera were computed in Excel and in
Stat graphic 4 (Windows XP) for statistical process-
ing. The data obtained on the nutrient media PDA and
MA have been pooled together. Only the samplings
paired per month have been evaluated for the
comparison between the years. Extreme values have
been excluded from data processing.
Analysis of variance (ANOVA) was employed to
test whether there are any significant differences in the
monthly mean concentrations of the total fungi and of
the genera Cladosporium,Penicillium,Aspergillus
and Alternaria between the years. In addition, the
Spearman rank order correlation coefficient (r
s
) was
used in order to compare the fluctuations of the daily
concentrations of the airborne fungi from year to year.
3 Results
3.1 Enumeration of samples
During the period of four years, a total of 6,600 Petri
dishes were exposed, during 562 sampling days (136,
142, 144 and 140 days during the years 1998, 1999,
2000 and 2001, respectively). A total of 70,583
colonies of fungi have been studied in the microscope,
identified and enumerated.
3.2 Diversity of fungi
One hundred and forty-nine taxa, representing 148
species and 1 variety, assigned into 54 genera, have
been identified. Additionally, the Basidiomycota, the
Sphaeropsidales, the yeasts and the NSF were
recorded as groups. Annually, 19 genera were
recorded during 1998, 45 genera in 1999, 39 in 2000
and 42 in 2001. Only 19 genera were constantly found
all the years, while 14 genera were rare and were
recovered in one out of the four years. The species
recovered (Table 1) are assigned to Zygomycota (8
species), Ascomycota (13 species) and anamorphic
fungi (127 species). Representative 320 strains of
filamentous fungi were isolated in pure culture and
maintained as reference material.
A great number of species were recognized in the
prevalent genera Cladosporium,Penicillium and
Aerobiologia
123
Table 1 List of fungal taxa isolated from the atmosphere of Athens during the years 1998–2001
Anamorphic fungi
Acremonium alternatum Link C. cladosporioides (Fresen.) de Vries
b
P. fellutanum Biourge
a
A. furcatum Moreau & R. Moreau ex
Gams
a
C. cucumerinum Ellis & Arthur
b
P. funiculosum Thom
b
A. murorum (Corda) W. Gams
a
C. herbarum (Pers.) Link
a
P. glabrum (Wehmer) Westling
b
Acrodontium griseum (Fassat.) de
Hoog
a
C. macrocarpum Preuss
b
P. glandicola (Oudem.) Seifert & Samson
a
A. virellum (Fr.) de Hoog
a
C. malorum Ruehle
a
P. implicatum Biourge
a
Alternaria alternata (Fr.) Keissl. C. oxysporum Berk. & Curt.
a
P. italicum Wehmer
A. citri Ellis & Pierce C. sphaerospermum Penz.
a
P. miczynskii K.M. Zalessky
a
A. infectoria Simmons
a
C. spongiosum Berk. & M.A. Curtis
a
P. olsonii Bainier & Sartory
a
A. tenuissima (Kunze) Wiltshire C. tenuissimum Cooke
a
P. oxalicum Currie & Thom
a
Arthrinium phaeospermum (Corda)
M.B. Ellis
a
C. variabile (Cooke) de Vries
a
P. pinophilum Thom
a
Aspergillus aculeatus Iizuka
b
Curvularia lunata (Wakker) Boedijn
a
P. purpurogenum Stoll
a
A. auricomus (Gue
´g.) Saito
a
C. lunata var. aeria
a
P. raistrikii G. Sm.
a
A. carbonarius (Bainier) Thom Dichobotrys abundans Hennebert
a
P. roqueforti Thom
a
A. clavatus Desm. Dicyma ampullifera de Lesd.
a
P. rugulosum Thom
a
A. flavus Link Doratomyces purpureofuscus (Schwein.)
F.J. Morton & G. Sm.
a
P. sclerotiorum J.F.H. Beyma
b
A. foetidus Thom & Raper
a
Drechslera halodes (Drechsler) Subram. &
B.L. Jain
a
P. solitum Westling
a
A. fumigatus Fresen. D. hawaiiensis (Bugnic.) Subram. & B.L.
Jain
a
P. thomii Maire
a
A.melleus Yukawa
a
D. tetramera (McKinney) Subram. & B.L.
Jain
a
P. verrucosum Dierckx
b
A. niger Tiegh. Epicoccum nigrum Link P. verruculosum Peyronel
a
A. niveus Blochwitz
a
Fusarium avenaceum (Fr.) Sacc.
a
Periconia sp.
A. ochraceus G. Wilh. F. dimerum Penz.
a
Pestalotiopsis sp.
A. oryzae (Ahlb.) E. Cohn
b
F. equisetii (Corda) Sacc.
a
Phoma glomerata (Corda) Wollenw. &
Hochapfel
a
A. ostianus Wehmer F. oxysporum Schltdl. Radulidium subulatum (de Hoog)
Arzanlou, W. Gams & Crous
a
A. parasiticus Speare
b
F. proliferatum (Matsush.) Nirenberg ex
Gerlach & Nirenberg
a
Rutola graminis (Desm.) J.L. Crane &
Schokn.
a
A. puniceus Kwong-Chung & Fennell
a
F. sporotrichoides Sherb.
a
Scopulariopsis brevicaulis (Sacc.) Bainier
b
A. sulphureus (Fresen.) Wehmer
a
Geotrichum candidum Link S. brumptii Salvanet-Duval
a
A. sydowii (Bainier & Sartory) Thom &
Church
a
Geotrichum sp. S. candida (Gue
´g.) Vuill.
a
A. terreus Thom Myrothecium sp. S. fusca Zach
a
A. tubingensis Mosseray
a
Nigrospora oryzae (Berk. & Broome)
Petch
b
Spiniger meineckellus (A.G. Olson)
Stalpers
a
A. ustus (Bainier) Thom & Church
b
Paecilomyces crustaceus (Apinis &
Chesters) Yaguchi
a
Sporotrichum pruinosum Gilman &
Abbott
a
A. versicolor (Vuill.) Tirab.
a
P. lilacinus (Thom) Samson
b
Stachybotrys chartarum (Ehrenb.) S.
Hughes
b
A. wentii Wehmer
b
P. marquandii (Massee) Hughes
a
S. parvispora S. Hughes
a
Aureobasidium pullulans (de Bary)
G. Arnaud
P. variotii Bainier
b
Stemphylium herbarum E.G. Simmons
b
Aerobiologia
123
Aspergillus (Table 1). The most common and abun-
dant species in the atmosphere of Athens were
Cladosporium cladosporioides,C. herbarum,Penicil-
lium chrysogenum,P. digitatum,Aspergillus niger,
A. ochraceus and Alternaria alternata. Other species
commonly recovered from the air were Cladosporium
oxysporum,C.tenuissimum,C.sphaerospermum,
Penicillium aurantiogriseum,P.brevicompactum,
P.citrinum,P.expansum,P.glabrum,P.italicum,
P.oxalicum,P.purpurogenum,P.thomii, Aspergillus
auricomus,A.flavus,A.ustus,A.parasiticus, as well
as Emericella and Eurotium species.
The number of fungal genera and species in the
atmosphere was increased during the warm months of
the year. The majority of the genera and the species
were recovered from May to November, except
Penicillium species that were found mainly during
the cold months of the year.
It is noteworthy that 12 species are reported from
the air for the first time worldwide (Table 2). The
occurrence of these fungi on other substrates may vary
from common to very rare, according to our estimate
based on data from literature. In addition, the species
Acremonium alternatum,Aspergillus melleus,Beau-
veria brogniartii,Chaetomium bostrychodes,
Chromelosporium fulvum,Cladobotryum varium,
Dichobotrys abundans,Doratomyces purpureofuscus,
Drechslera halodes,Fusarium dimerum,Paecilomy-
ces marquandii,Penicillium miczynskii,Penicillium
pinophilum,Penicillium raistrikii,Radulidium subul-
atum and Scopulariopsis fusca have been rarely
reported from the air.
Table 1 continued
Beauveria bassiana (Bals.-Criv.) Vuill.
a
Penicillium aurantiogriseum Dierckx
a
Torula herbarum (Pers.) Link
a
B. brongiartii (Sacc.) Petch
a
P. brevicompactum Dierckx
a
Trichoderma viride Pers.
Botryosporium longibrachiatum
(Oudem.) Maire
a
P. chrysogenum Thom Trichothecium roseum (Pers.) Link
Botrytis cinerea Pers. P. citrinum Thom Ulocladium alternariae (Cooke) E.G.
Simmons
a
Chromelosporium fulvum (Link)
McGinty
a
P. commune Thom
a
U. atrum Preuss
a
Chrysonilia sitophila (Mont.) Arx.
a
P. crustosum Thom
a
U. botrytis Preuss
a
Cladobotryum varium Nees
a
P. decumbens Thom
a
Verticillium albo-atrum Reinke &
Berthold
b
Cladosporium breviramosum Morgan-
Jones & B.J. Jacobsen
a
P. digitatum (Pers.) Sacc. V. luteoalbum (Link) Subram.
a
C. chlorocephalum (Fresen.)
E.W. Mason & M.B. Ellis
a
P. expansum Link
b
Zygosporium masonii S. Hughes
a
Ascomycota
Chaetomium bostrychodes Zopf
b
E. intermedium Blaser
a
Petromyces alliaceus Malloch & Cain
c
C. globosum Kunze E. rubrum Jos. Ko
¨nig et al.
a
Sclerotinia sclerotiorum (Lib.) de Bary
a
Emericella nidulans (Eidam) Vuill. Neosartorya fischeri (Wehmer) Malloch &
Cain
a
Talaromyces flavus (Klo
¨cker) Stolk &
Samson
a
E. variecolor Berk. & Broome
a
Petriella guttulata Barron & Cain
a
Eurotium amstelodami L. Mangin
a
Petriella sp.
Zygomycota
Circinella minor Lendn.
a
Mucor plumbeus Bonord.
a
Rhizopus oryzae Went & Prins. Geerl.
b
C. umbellata Tiegh. & Le Monn.
a
M. circinelloides Tiegh.
a
Syncephalastrum racemosum Cohn ex
Schro
¨t.
a
Cunninghamella echinulata
(Thaxt.)Thaxt. ex Blakes.
b
M. racemosus Fresen.
a,b
Taxa reported for the first and second time, respectively on any substrate from Greece
c
Teleomorph reported for the first and anamorph for the second time on any substrate from Greece
Aerobiologia
123
The majority of the species are reported from
Greece for the first time as airborne. Also, 19 genera
and 93 species are reported for the first time, and 11
genera and 23 species, for the second on any substrate
(Table 1).
3.3 Abundance of fungi
The airborne mycobiota presented fluctuations in
daily, monthly and seasonal concentrations in each
year. The annual mean concentration of the total fungi
was 538, 640, 694 and 638 CFU/m
3
for the years 1998,
1999, 2000 and 2001, and the concentration range was
25–2,435, 117–2,822, 122–2,201 and 116–2,590 CFU/m
3
,
respectively. Detailed data are presented in the
Tables 3and 4.
The vast majority of the airborne fungi recovered
during the 4 years were anamorphic (75%), followed
by the NSF (13.8%), the yeasts (8.5%), Ascomycota
(1.3%), Basidiomycota (1.2%) and Zygomycota
(0.3%).
The genera Cladosporium,Penicillium,Aspergillus
and Alternaria predominated in descending order, in
the atmosphere of Athens.
The monthly fluctuations of the total fungi and the
predominant genera for the 4 years are presented in
Fig. 1. The total fungi presented increased concentra-
tions from May to July and from October to Novem-
ber. The peak recorded in February 1999 was due to
the high numbers of Penicillium spores during that
time.
The genus Cladosporium was the dominant com-
ponent, except during the year 1999 when it was
surpassed by the genus Penicillium. The concentration
of Cladosporium spores exhibited a major peak from
May to July, and a lower one, during October. The
spores of the genus Penicillium decreased significantly
during summer months in all the 4 years of the study.
Very high concentrations of Penicillium were
recorded during February 1999. A spore shower of
Penicillium was recorded on 25-02-1999 with a
concentration of 10,393 CFU/m
3
as an extreme value.
The genus Aspergillus increased during the warm
months of the year with maximum values during
September and October. The genus Alternaria was
encountered in high concentrations from May until
August with maximum concentrations in June or July.
The NSF and the yeasts exhibited no evident seasonal
patterns, except an increase in the yeasts during the
winter months of the first 2 years.
The genera Cladosporium,Penicillium,Aspergillus
and Alternaria as well as the NSF and the yeasts have a
frequency of 100% and were present in high concen-
trations during all the sampling days (Table 3). They
are considered as dominant and stable components of
the Athens bioaerosol. The Basidiomycota and the
Sphaeropsidales, as well as the genera Acremonium,
Arthrinium,Aureobasidium,Botrytis,Emericella,
Epicoccum,Eurotium,Fusarium,Geotrichum,Mucor,
Paecilomyces,Rhizopus,Scopulariopsis,Spiniger,
Stachybotrys and Ulocladium, may be considered as
common. They have been recovered roughly with a
frequency of 10–50%, an AMC 1–10 CFU/m
3
and a
percentage of 0.1–1% in the total. There were also
found thirty-three genera sporadically recovered in
even lower frequency and concentration, and they are
regarded as uncommon. A few of them are rare since
they were found only once or twice in the 4-year
period, and it is most unlikely to be recovered.
3.4 Statistical analysis
A statistical analysis has been applied for the
comparison of the airborne fungi qualitatively and
quantitatively from year to year. The dominant and
stable components of the Athens atmosphere were the
same in all the 4 years. Only the sporadic and rare
genera were different from year to year. Analysis of
variance (ANOVA) was applied to compare the
difference in the monthly mean concentration from
Table 2 Species newly reported as airborne
Species Occurrence
a
Acrodontium virellum Rare
Aspergillus aculeatus Uncommon
Aspergillus tubingensis Rare
Circinella minor Common
Circinella umbellata Common
Cladosporium breviramosum Very rare
Cladosporium malorum Common
Drechslera tetramera Common
Paecilomyces crustaceus Common
Petriella guttulata Very rare
Rutola graminis Rare
Sporotrichum pruinosum Common
a
On any substrate
Aerobiologia
123
Table 3 Qualitative and quantitative data of the airborne mycobiota recovered each year of the study
Genus or group 1998 1999 2000 2001
AMC CFU/m
3
%F(%) AMC CFU/m
3
%F(%) AMC CFU/m
3
%F(%) AMC CFU/m
3
%F(%)
Acremonium 0.46 0.07 7.75 1.89 0.28 22.917 1.26 0.20 18.57
Acrodontium 0.29 0.046 4.93 0.11 0.016 2.78 0.20 0.03 5
Alternaria 34 6.32 83.82 32.99 5.22 100 32.03 4.69 100 32.34 5.15 100
Arthrinium 3.25 0.60 9.56 1.15 0.18 18.31 1.69 0.25 25 1.51 0.24 23.57
Aspergillus 36.52 6.79 100 55.31 8.68 100 60.15 8.82 100 50.26 8.01 100
Aureobasidium 5.20 0.97 20.59 3.73 0.59 44.37 6.35 0.93 63.89 5.06 0.81 55.71
Beauveria 0.06 0.009 1.41 0.14 0.02 2.08 0.29 0.05 4.29
Botryosporium 0.03 0.005 0.70 0.08 0.012 1.39
Botrytis 4.78 0.89 17.65 2.23 0.35 30.28 1.50 0.22 24.31 2.01 0.32 31.43
Chaetomium 0.23 0.036 4.93 0.76 0.11 12.5 0.40 0.06 9.29
Chromelosporium 0.03 0.004 0.69
Chrysonilia 0.09 0.018 0.74 0.09 0.013 2.11 0.03 0.004 0.69 0.09 0.014 2.14
Circinella 0.06 0.009 1.41 0.11 0.016 2.78 0.17 0.03 4.29
Cladobotryum 0.03 0.005 0.71
Cladosporium 200.13 37.21 100 120.43 19.07 100 250.22 36.67 100 254.02 40.49 100
Cunninghamella 0.06 0.009 0.70 0.03 0.004 0.69 0.03 0.005 0.71
Curvularia 0.11 0.018 1.41
Dichobotrys 0.09 0.014 1.43
Dicyma 0.03 0.005 0.70 0.03 0.004 0.69 0.03 0.005 0.71
Doratomyces 0.11 0.018 2.82 0.19 0.028 4.17 0.11 0.018 2.86
Drechslera 0.18 0.03 0.74 0.20 0.03 4.93 0.22 0.033 4.86 0.09 0.014 2.14
Emericella 5.56 0.88 47.18 8.11 1.19 45.8 6.04 0.96 43.57
Epicoccum 1.58 0.29 7.35 0.77 0.12 11.27 1.26 0.19 22.22 1.39 0.22 19.29
Eurotium 2.49 0.39 28.87 3.38 0.49 40.27 4.73 0.75 48.57
Fusarium 2.04 0.38 8.82 1.38 0.22 23.24 1.18 0.17 20.14 1.67 0.27 26.43
Geotrichum 0.80 0.13 11.27 0.81 0.12 18.75 2.20 0.35 27.86
Mucor 0.40 0.075 2.21 1.42 0.22 21.13 0.74 0.11 9.72 0.40 0.06 9.29
Myrothecium 0.09 0.014 0.71
Neosartorya 0.03 0.005 0.70
Aerobiologia
123
Table 3 continued
Genus or group 1998 1999 2000 2001
AMC CFU/m
3
%F(%) AMC CFU/m
3
%F(%) AMC CFU/m
3
%F(%) AMC CFU/m
3
%F(%)
Nigrospora 0.09 0.018 0.74 0.09 0.013 2.11 0.11 0.016 2.78
Paecilomyces 8.32 1.55 14.71 3.44 0.55 31.69 1.62 0.24 24.31 1.01 0.16 20
Penicillium 96.61 17.97 100 194.48 30.79 100 165.76 24.29 100 120.14 19.15 100
Periconia 0.09 0.014 1.43
Pestalotiopsis 0.11 0.019 0.70 0.03 0.004 0.69
Petriella 0.09 0.014 1.43
Petromyces 0.46 0.07 8.45 0.03 0.004 0.69 0.09 0.014 2.14
Phoma 0.09 0.014 0.71
Radulidium 0.03 0.005 0.70
Rhizopus 0.55 0.10 2.21 2.37 0.05 28.87 1.75 0.26 30.56 1.56 0.25 26.43
Rutola 0.09 0.013 1.41
Sclerotinia 0.24 0.045 1.47 0.32 0.05 3.52 0.22 0.033 4.17 0.11 0.018 2.86
Scopulariopsis 0.24 0.044 2.94 0.56 0.09 13.38 1.68 0.25 30.56 1.36 0.22 22.86
Spiniger 0.31 0.05 6.34 1.76 0.26 15.97 1.24 0.20 17.86
Sporotrichum 0.06 0.009 1.41
Stachybotrys 0.37 0.06 8.45 0.42 0.06 9.03 0.74 0.12 17.14
Stemphylium 0.19 0.03 4.93 0.11 0.016 2.78 0.03 0.005 0.71
Syncephalastrum 0.03 0.005 0.70
Talaromyces 0.03 0.005 0.71
Torula 0.09 0.014 2.14
Trichoderma 0.25 0.047 0.74 0.31 0.05 6.34 0.36 0.05 6.95 0.29 0.05 7.14
Trichothecium 0.09 0.013 2.11 0.11 0.018 2.86
Ulocladium 3.00 0.56 11.03 1.13 0.18 20.42 1.54 0.22 21.53 0.95 0.15 19.29
Verticillium 0.03 0.005 0.70 0.06 0.008 1.39
Zygosporium 0.06 0.009 1.41 0.06 0.008 1.39
Basidiomycota 9.93 1.57 11.27 1.85 0.27 9.03 18.31 2.92 36.43
Sphaeropsidales 7.97 1.48 12.50 4.45 0.70 52.82 7.24 1.06 65.97 4.94 0.79 52.86
Yeasts 69.54 12.93 100.00 73.28 11.6 100 38.92 5.70 100 30.12 4.80 100
Unidentified fungi 1.89 0.35 2.94 20.98 3.32 69.72 5.31 0.78 56.94 2.01 0.32 22.14
Aerobiologia
123
year to year for Cladosporium,Penicillium,Aspergil-
lus,Alternaria and the total fungi. The results of the
analysis are presented in Table 5. Since the P
value
of
the Ftest is greater than 0.05 for the total fungi and for
the genera Penicillium and Aspergillus, there is not a
statistically significant difference at the 95.0% confi-
dence interval between the monthly mean concentra-
tions of the 4 years. On the contrary, the P
value
is lower
than 0.01 for the genera Cladosporium and Alternaria;
therefore, there is a statistically significant difference
at the 99.0% confidence interval among the mean
concentrations of the 4 years.
The Spearman rank order correlation coefficient
(r
s
) was applied to test the fluctuations of the daily
concentrations exhibited by the total fungi and the
dominant genera between the sampling years, and the
results are presented in Table 6. The annual fluctua-
tions of the total fungi and of the genera Cladosporium
and Penicillium were weakly to moderately correlated
and of the genera Aspergillus and Alternaria more
strongly correlated between the years. Most of the
correlations are statistically significant (Table 6).
4 Discussion
The aeromycological investigations are increasingly
concerned with the air quality in the indoor environ-
ments, often supplemented by the study of the ambient
air for a comparison. The majority of the airborne
fungi remain unidentified at the species level, since the
diversity is not usually a priority in the research
objectives. Most of the studies are focusing on those
fungi which potentially may cause adverse health
effects, so that the rest are underestimated or over-
looked. For example, during an extensive survey on
the indoor fungi compared to outdoor fungi in USA, a
detailed account at the genus level is provided but only
species of medical importance have been identified
(Shelton et al. 2002).
Actually, there is a multifaceted influence of fungi
in human affairs. The knowledge on the occurrence of
fungi in any particular ecological niche is of great
importance, and this is especially true concerning the
atmosphere, which permits the effective dissemination
of the fungal propagules and ensures their establish-
ment on new substrates.
This study offers novel information about the
diversity of the airborne fungi. One hundred and
Table 3 continued
Genus or group 1998 1999 2000 2001
AMC CFU/m
3
%F(%) AMC CFU/m
3
%F(%) AMC CFU/m
3
%F(%) AMC CFU/m
3
%F(%)
NSF 60.91 11.33 100 97.24 15.39 100 94.01 13.78 100 90.52 14.43 100
TOTAL FUNGI 537.81 639.82 693.85 638.26
AMC, annual mean concentration (average of the daily concentrations. CFU/m
3
); % percentage of each genus or group relatively to the total number of fungi; Ffrequency of
recovery (% number of days the fungi were recovered out of 136 days of sampling in 1998, 142 days of sampling in 1999, 144 days of sampling in 2000 and 140 days of
sampling in 2001)
Aerobiologia
123
forty-eight species in fifty-four genera of filamentous
fungi have been isolated and studied in pure culture.
This seems to be a higher number of airborne fungal
species than ever before recovered from a single site.
A higher number has been recovered from two sites in
Turin, where 165 species of mesophilic fungi and
some more thermotolerant were recorded (Airaudi &
Filipello Marchisio 1996). A high diversity was also
found in Kuwait with 116 species recorded from one
site (Moustafa and Kamel 1976), in Egypt with 102
species from six regions (Ismail et al. 2002) and 83
species from a desert locality (Abdel-Hafez and
El-Said 1989) and in Qatar with 73 species (Al-Subai
2002). In a study including multiple sites in five cities
of Lithuania, 430 species of fungi have been reported,
but only part of them is listed by name (Lugauskas
et al. 2003).
In the genera Penicillium and Aspergillus, 29 and
30 species, respectively, have been recovered. Anal-
ogous high species diversity in these genera has been
reported in the Mediterranean region, from Italy
(Airaudi and Filipello Marchisio 1996) and Spain
(Herrero et al. 1996). Moreover, twelve species of
Cladosporium have been recovered from the Athens
atmosphere, and this is at least twice the number of
species found in other geographic areas. The most
frequent and abundant species were C. cladosporio-
ides and C. herbarum as also reported from Turin
(Filipello Marchisio et al. 1992) and Barcelona (Calvo
Torras et al. 1981).
Most of the species recovered in Athens are
cosmopolitan and have been reported from several
regions around the world. However, 29 species are
considered to be rare in the air, as well as 12 species
are reported from the air for the first time worldwide.
Some of the species are very rare in any environ-
ment and in any substrate. One of the most intriguing
findings was Cladosporium breviramosum, which was
only known from its original description in Georgia in
the United States, on hotel wallpaper (Morgan-Jones
and Jacobsen 1988).
The majority of the species are reported as airborne
for the first time in Greece. Also, 19 genera and 93
species are reported for the first time, and 11 genera
and 23 species for the second time, from any substrate
in Greece.
All the fungal strains isolated from the air have
been maintained as reference material for future
studies. The ATHUM Culture Collection, with a focus
on airborne fungi (Kapsanaki-Gotsi 2001), has
increased its holdings by 320 strains, representing
148 species in 54 genera of filamentous fungi. Some of
these strains are unique or rarely found in other
Culture Collections.
The airborne fungi do not show significant variation
in concentration from year to year, as statistically
tested by the comparison of the data recovered each
sampling year. The annual mean concentration (AMC)
of the total fungi in Athens during the 4 years ranged
from 538 to 694 CFU/m
3
. There are not enough data
available on the AMC of the total airborne fungi
studied by a viable volumetric method, from other
geographic regions. Higher mean concentrations have
been reported from Dublin, Ireland, with 915 CFU/m
3
(O’Gorman and Fuller 2008), from Beijing, China,
with 1,165 CFU/m
3
(Fang et al. 2005) and from USA,
with 930 CFU/m
3
(Shelton et al. 2002). The concen-
tration range of the total fungi in Athens during the
4 years was 25–2,822 CFU/m
3
and is quite similar to
the spore range recorded in Yokohama, Japan
(Takahashi 1997). Higher maximum concentrations
from other urban areas have been reported from Turin,
Italy (Filipello Marchisio and Airaudi 2001), from
Beijing, China (Fang et al. 2005), from USA (Shelton
Table 4 Concentration
range of the total fungi and
of the predominant genera
for each sampling year
* 10,393 CFU/m
3
was
recorded on 25-02-1999, an
extreme value excluded
from statistical analysis
Fungal taxa Concentration range (CFU/m
3
)
1998 1999 2000 2001
Total Fungi 25–2,435 116–2,822 122–2,201 116–2,590
Cladosporium 8–2,169 8–1,703 4–1,945 13–2,202
Penicillium 13–1,068 4–864* 8–1,218 8–701
Aspergillus 8–204 8–542 4–404 4–642
Alternaria 4–180 4–271 4–179 4–235
Aerobiologia
123
0
200
400
600
800
1000
1200
CFU/m
3
JFMAMJJASOND
1998
1999
2000
2001
MONTHS
TOTAL FUNGI
0
100
200
300
400
500
600
CFU/m
3
1998
1999
2000
2001
MONTHS
CLADOSPORIUM
0
100
200
300
400
500
600
1998
1999
2000
2001
MONTHS
PENICILLIUM
0
50
100
150
200
1998
1999
2000
2001
MONTHS
ASPERGILLUS
0
50
100
150
200
1998
1999
2000
2001
MONTHS
ALTERNARIA
0
50
100
150
200
250
300
350
400
1998
1999
2000
2001
MONTHS
YEASTS
0
50
100
150
200
250
300
350
400
JFMAMJJASON
D
JFMAMJJASOND
J FMAMJ J A SOND J FMAMJ J A SOND
J FMAMJ J A SOND J FMAMJ J A SOND
1998
1999
2000
2001
MONTHS
NON SPORULATING FUNGI
CFU/m
3
CFU/m
3
CFU/m
3
CFU/m
3
CFU/m
3
1998 1999 2000 2001
1998 1999 2000 2001 1998 1999 2000 2001
1998 1999 2000 2001 1998 1999 2000 2001
1998 1999 2000 2001
1998 1999 2000 2001
Fig. 1 Fluctuations of the monthly mean concentration of the total fungi and the predominant components, during the years 1998,
1999, 2000 and 2001
Aerobiologia
123
et al. 2002; Tsai et al. 2007), from Buenos Aires,
Argentina (Negrin et al. 2007), and from Taiwan
(Huang et al. 2002; Wu et al. 2007).
The genera Cladosporium,Penicillium,Aspergillus
and Alternaria, the yeasts and the NSF were the major
constituents of the fungal aerosol. They were recov-
ered in high concentrations with a frequency of 100%
and are considered as dominant and stable components
of the Athens atmosphere. These fungi are also
prevalent, although in various quantities, in other
Mediterranean countries (Calvo et al. 1980a;
El-Morsy 2006; Filipello Marchisio and Airaudi
2001; Roses-Codinachs et al. 1992) in North Europe
(Larsen & Gravesen 1991; O’Gorman and Fuller
2008), in Asia (Adhikari et al. 2004; Fang et al. 2005;
Takahashi 1997) and America (Negrin et al. 2007;
Shelton et al. 2002).
The total fungi and the major components exhibited
seasonal fluctuations during each year. The concentration
of the total fungi was increased twice in a year,
mainly from May to July and from October to
November. Seasonality with two peaks has been
reported from Beijing, China (Fang et al. 2005), and
West Bengal, India (Das and Gupta-Bhattacharya
2008). A single peak has been recorded, either during
the summer time, in Italy (Filipello Marchisio et al.
1997), Austria (Ebner et al. 1992), Ireland (O’Gorman
and Fuller 2008), USA (Tsai et al. 2007) and Japan
(Takahashi 1997), or during the winter time, in Saudi
Arabia (Al-Suwaine et al. 1999) and Taiwan (Huang
et al. 2002).
The dominant genus Cladosporium, which mostly
defines the total, has also presented a double peak, one
from May to July and the second during October. An
analogous pattern has been reported in Turin (Filipello
Marchisio et al. 1997; Filipello Marchisio and Airaudi
2001). The genus Penicillium increased significantly
during the winter months. The extraordinary rise of
Penicillium in February 1999 can be attributed to the
accumulation of trash in the streets around the city
center, due to a prolonged strike of sanitation workers.
The genus Aspergillus did not similarly rise due to the
trash, since the low temperatures are usually unfavor-
able for its growth. The concentration of the genus
Aspergillus was increased during summer and mark-
edly peaked in autumn months. Similar distributions
for Penicillium and Aspergillus were reported in
Denmark (Larsen and Gravesen 1991) and in Saudi
Arabia (Al-Suwaine et al. 1999). The concentration of
the genus Alternaria was significantly higher from
Table 5 Comparison of the annual mean concentration of the
total fungi and of the predominant genera
Fungal taxa ANOVA
F-ratio P
value
Total fungi 0.30 0.88
Cladosporium 7.22 0.00*
Penicillium 0.69 0.56
Aspergillus 0.60 0.61
Alternaria 7.89 0.00*
* Statistically significant difference
Table 6 Correlation of the seasonal fluctuations of the total fungi and of the predominant genera exhibited each sampling year
Fungal taxa r
s
P
value
1998–1999 1999–2000 2000–2001 1998–2000 1999–2001 1998–2001
Total fungi 0.043 -0.067 0.196 0.166 -0.105 0.351
0.641 0.428 0.021* 0.113 0.216 0.000*
Cladosporium 0.114 0.087 0.442 0.266 0.060 0.573
0.227 0.305 0.000* 0.005* 0.479 0.000*
Penicillium 0.137 0.308 0.213 0.158 0.247 0.160
0.172 0.000* 0.012* 0.115 0.003* 0.111
Aspergillus 0.278 0.435 0.366 0.207 0.452 0.306
0.013* 0.000* 0.000* 0.064 0.000* 0.006*
Alternaria 0.151 0.574 0.588 0.223 0.531 0.434
0.191 0.000* 0.000* 0.053 0.000* 0.000*
* Statistically significant correlations
Aerobiologia
123
May to October. An analogous pattern for Alternaria
was found in Italy (Filipello Marchisio et al. 1992,
1997,2001), Austria (Ebner et al. 1992), Denmark
(Larsen and Gravesen 1991), China (Fang et al. 2005)
and Japan (Takahashi 1997).
The yeasts and the NSF, which were stable
components of the fungal aerosol, although variable,
had not presented clear seasonal patterns.
It is worth mentioning that the first year of sampling
did not show a significant difference from the follow-
ing years, concerning the fluctuation in the concen-
trations of the total fungi and the prevalent genera,
although there was a deficiency in the sampling media
during the first year. Nevertheless, fewer genera were
found during the first year, which may be due to the
medium or may be partly considered as a matter of
chance. Fourteen genera, which were recovered in
inconsiderable concentration, only once or twice
during the whole period of the 4 years, were absent
during the first year.
It has to be appreciated that the taxa recovered
during this study represent only a small proportion of
those actually present in the atmosphere, due to
intrinsic limitations of the methodology and also to the
difficulty of obtaining slow-growing species that are
often masked by the overgrowth of the more compe-
tent fungi. Also, the concentration of the fungal
propagules recovered is underestimated by the cultural
method, since a lot of the spores have lost their
viability or may be unculturable such as rust and smut
spores (Pyrri and Kapsanaki-Gotsi 2007a).
The diversity of fungi in the air particulate matter is
higher than expected, as revealed by molecular
analysis (Fro
¨hlich-Nowoisky et al. 2009). The pres-
ence and mass concentrations of fungal spores in the
aerosols may be more significant than currently
known, and they can influence even the atmospheric
processes (Bauer et al. 2008).
The studies on the occurrence and abundance of the
airborne fungi in a global scale, by conventional
methods supplemented by molecular approaches, will
result in an improvement of the monitoring strategy
and in a more complete evaluation of the importance
of fungi. Furthermore, they will contribute to the
understanding of the multiple roles and complicated
pathways held by the mycobiota in natural and man-
made ecosystems, since most of the fungi get the
opportunity to establish themselves in new territories,
by their launching into the atmosphere.
Acknowledgments We thank the Curators of the BPIC, CBS,
CCF, FRR, MUCL, NRRL and UAMH Culture Collections,
who allowed access to fungal strains included in their holdings.
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