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Concentrations and dynamics of fungal spore

populations in the air of Zarqa, Jordan, using the
volumetric method
a b
Mohammed H. Abu-Dieyeh & Raghda Barham
a
Department of Biological and Environmental Sciences, College of Arts and Sciences,
Qatar University, Doha, Qatar
b
Department of Biology and Biotechnology, The Hashemite University, Zarqa, Jordan
Published online: 01 May 2014.

To cite this article: Mohammed H. Abu-Dieyeh & Raghda Barham (2014) Concentrations and dynamics of
fungal spore populations in the air of Zarqa, Jordan, using the volumetric method, Grana, 53:2, 117-132, DOI:
10.1080/00173134.2014.896413

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 Grana, 2014
Vol. 53, No. 2, 117–132, http://dx.doi.org/10.1080/00173134.2014.896413

Concentrations and dynamics of fungal spore populations in the air of

Zarqa, Jordan, using the volumetric method

MOHAMMED H. ABU-DIEYEH1 & RAGHDA BARHAM2

1
Department of Biological and Environmental Sciences, College of Arts and Sciences, Qatar University, Doha, Qatar,
2
Department of Biology and Biotechnology, The Hashemite University, Zarqa, Jordan
Downloaded by [York University Libraries] at 05:36 12 August 2014

Abstract
This study was initiated to investigate seasonal and intradiurnal variations in concentrations of airborne fungal spores of the
Zarqa area in Jordan based on daily spore trapping. A total of 76 396 fungal spores belonging to 41 genera of fungi were
identified. The maximum trapped fungus was Cladosporium (49.39%) followed by Puccinia uredospores (11.14%), Alternaria
(7.70%), Ustilago (7.62%) and Drechslera (4.03%). The remainder (20.12%) was attributed to 36 genera of fungi. April was
the month with the highest mean daily concentration (27.82 spores/m3), while January was the lowest. Two peaks were
recorded, one in April (139.58 spores/m3) and another in June (70.42 spores/m3). Total daily spore counts showed
significant positive correlations with maximum and mean temperature and a significant negative correlation with relative
humidity. The monthly mean and the total annual counts of fungal spores were both significantly favoured the period 20.00–
04.00. It was suggested that results of spore trapping and settle plate exposures (a previous study) can be complementary but
not comparable except in the fact that Cladosporium was the most common fungi in both. Most of the recorded fungi have
been reported as allergenic or pathogenic for humans, animals and plants, therefore further research on ecological,
economical and medical aspects should be encouraged.

Keywords: aerospora, aeromycology, seasonal and diurnal dynamics, spore trap, arid land

Aeromycological knowledge is of primary impor- increased public awareness of the importance of

tance to plant pathologists, allergists and aerobiolo-
gists. Airborne fungal spores have been implicated
in the induction of plant diseases and are responsi-
ble for considerable distresses in people who show
allergic reactions to fungal spores (Romanet-
Manent et al. 2002). The prevalence of respiratory
allergy to fungi is estimated to be 20–30% among
individuals; these numbers can be somewhat smal-
ler in different climatic zones (Breitenbach et al.
2002). The suffering of older patients from allergic
asthma is particularly due to fungal infections of the
lung, which is the major allergic manifestation
induced by fungi (O’Hollaren et al. 1991).
Moreover, fungal toxins still represent important
health problems for humans, animals and plants
(Bhatnagar et al. 2000). This situation has led to
indoor and outdoor air quality.
There are only two published aeromycological stu-
dies from Jordan, i.e. one that was conducted in the
Amman area using a seven-day volumetric spore trap
(Shaheen 1992) and another one, which was recently
published concerning the Zarqa area using the settle
plate exposure method (Abu-Dieyeh et al. 2010). Due
to the fact that the settle plate exposure method had
some limitations and concealed a portion of the air-
borne microorganisms (Moustafa & Kamel 1976;
Mitakakis & Guest 2001; Ho et al. 2005), a seven-day
recording volumetric spore trap was used instead to
conduct the present study in order to: (1) survey air-
borne fungal spores in the atmosphere of the Zarqa
area for a period of one year starting from December
2008 until the end of November 2009; (2) investigate

Correspondence: Mohammed H. Abu-Dieyeh, Department of Biological and Environmental Sciences, College of Arts and Sciences, Qatar University, P. O.
Box: 2713, Doha, Qatar. E-mail: dandelion@qu.edu.qa

(Received 31 May 2013; accepted 18 December 2013)

© 2014 Collegium Palynologicum Scandinavicum

 118 M. H. Abu-Dieyeh and R. Barham
variations in seasonal and intradiurnal distribution of
airborne fungal spores and to correlate these variations
with meteorological factors; (3) compare the volu-
metric data with the settle plate exposure data obtained
from the previous study.
Material and methods
Study area
Jordan is situated about 100 km from the south-east-
ern coast of the Mediterranean Sea, between lati-
tudes 29°–33° N and longitudes 35°–39° E. It has a
land area of about 89 200 km2, of which arable land
is less than 5%. The present study was conducted at
the campus of The Hashemite University, Zarqa
(32° 04' N, 36° 12' E; 550–650 m above sea level),
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which is situated 40 km east of Amman. The mean
annual precipitation is approximately 115 mm,
occurring mainly between October and April. The
recorded temperature ranges between 0.0 °C in
December/January to around 40 °C recorded in
July/August. The mean minimum temperature in
winter is 2.7 °C and the mean maximum tempera-
ture in summer is 34.3 °C. The prevailing wind
direction is northwest (NW) with a mean monthly
wind speed ranged between 3.7 and 14.5 km/h.
According to bioclimatic classification, the area is
specifically classified as arid Mediterranean, while
the vegetation type is typically an Irano-Turanian
(steppe) region (Zohary 1962; Al-Eisawi 1985).
The area is mainly formed by rocky limestone
hills, flat plains and broad wadis. The natural vege-
tation is predominantly formed by bushes such as
Salsola baryosma (Roem et Schult) Dandy, Noaea
mucronata Asch. et Schweinf., Hammada scoparia
(Pomel) Iljin, Anabasis syriaca Iljin and Artemisia
herba-alba Asso. Retama raetum Webb et Berthel.
shrubs represent the climax vegetation in the hilly
areas. Recently, the area became highly populated
due to the construction of many housing projects,
university campuses and investment activities for
industrial, commercial and service purposes.
The region is highly industrialised with more than
52% of Jordanian industry located in Zarqa. These
include the main oil refinery, the King Hussain
Thermal Power Plant and other chemical industries.
Moreover, Kherbit El-Samra, the main wastewater
treatment plant in the country that treats about 80%
of municipal and industrial wastewater, and Al-Rusaifa
Landfill, which is considered as the largest landfill in
Jordan, are located within the region as well. New
agricultural projects accompanied the above develop-
ment. In the campus of The Hashemite University,
around 8–15 years ago, olive trees were planted in the
plains and on low slopes covering around 100 ha.
Ornamental shrubs and trees are also planted on the
hill slopes, along roads and near the buildings, includ-
ing Pinus sp., Casuarina sp., Cupressus sp., Eucalyptus
sp. and Ceratonia sp. A variety of ruderal annuals and
weeds grow under and between ornamental and olive
trees. The dominant weed species are Diplotaxis eru-
coides (L.) DC., Eruca sativa Mill., Sonchus oleraceus L.,
Malva neglecta Wallr. and Chenopodium album L.
Trapping method and slide preparation
This study was based on the trapping method using
the Burkard seven-day recording volumetric spore
trap (Burkard Manufacturing Co. Ltd, London,
UK). The spore trap was installed on the roof of
the University’s Biological Science Department
building, which is about 12 m above ground level.
At 12.30 on Sunday and every week of the sampling
period (a whole year from 1 December 2008 until 30
November 2009), the drum was properly replaced
(see Hirst 1952). Each week and directly after drum
removal, the collected Melinex tape (Burkard
Manufacturing Co. Ltd, London, UK) was marked,
segmented (each segment represents a 24-hour-per-
iod) and then placed on previously labelled micro-
scopic slides. Glycerine jelly was added as a
mounting medium. Slides were then covered by
cover slips (52 mm × 22 mm) and stored horizontally
in a slide cabinet until dry.
Identification and counting of airborne fungal spores
Reference culture plate collections for airborne fungi
from air of Zarqa were stored from a previous work
(Abu-Dieyeh et al. 2010). The fungal cultures were
subjected to long-storage under freezing conditions
(–20 °C). Wet mounts from these cultures were pre-
pared, examined under the microscope and then
photographed using a digital camera attached to a
compound light microscope (Labomed, Fremont,
CA, USA). The pictures were stored for future use
as references to identify trapped fungal spores.
Several keys, atlases and pictures (Nilsson 1983;
Shaheen 1989; Moubasher 1993; Samson et al.
2002) were considered as the base for spore identifi-
cation. The trapped fungal spores were classified to
genus level; spores that were difficult to be classified
were grouped as ‘Unknown’.
The whole area of each slide representing a 24-
hour period was completely scanned; thus identify-
ing and counting all the fungal spores encountered.
Based on daily counts and the air flow per time of the
spore trap, monthly and yearly counts and fungal
spore concentrations were calculated and statistically
analysed. To assess diurnal variation of airborne
fungal spores in the atmosphere of the Zarqa area,

the day time was divided into three eight-hour-peri-
ods ranging from 12.00–20.00, 20.00–04.00 and
04.00–12.00. The total daily counts of fungal spores
trapped during each period for a whole month were
summed up in tables.
Meteorological data
Daily meteorological data from the Zarqa weather
station were supplied by the Weather Record
Department, Amman. The considered meteorologi-
cal data include minimum and maximum daily tem-
perature, minimum and maximum relative humidity,
daily rainfall, wind direction and wind speed.
Statistical analysis
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The data were subjected to a Shapiro–Wilk test and
found to be normally distributed. Statistical analyses
were performed to correlate the mean daily fungal
spore concentrations with the data of the meteorolo-
gical parameters of the same day using the Pearson
correlation coefficient. Data for diurnal study were
analysed using one-way analysis of variance
(ANOVA) and means of variables were separated
using Tukey’s test at P ≤ 0.05 (SigmaStat 3.5,
Systat Software, Inc., Chicago, IL, USA).
Results
Annual spores count
From the entire study, a total of 76 396 fungal spores
belonging to 41 genera of fungi were identified. The
most common trapped fungus was Cladosporium with
a percentage of almost half of the total airborne
fungal spores (49.39%) and Spegazzinia was the
fungus with lowest percentage (0.02%; Table I).
The other common fungal spores in the atmosphere
of Zarqa are Puccinia uredospores (11.14%),
Alternaria sp. (7.70%), Ustilago sp. (7.62%) and
Drechslera sp. (4.03%). The remainder (20.12%)
was attributed to all other fungi (represent 36 gen-
era) including the unknown group of spores.
Deuteromycota obtained the highest percentage
(72.3%) followed by Basidiomycota (20.6%),
Ascomycota (6.5%) and then Zygomycota (0.6%)
(Table I).
Daily and monthly fungal spore counts and
concentrations
A rush period of fungal spores was obtained from
April to August, which represents 62.5% of the total
spores collected in the year of study (Table I). April
had the maximum value of fungal spores in the
Fungal airborne spores of Jordan (Zarqa) 119
atmosphere of the Zarqa area (12 017 spores) while
January had the minimum value (3066 spores).
According to maximum daily concentration, two
peaks appeared, one in April (140 spores/m3) and
another in June (70 spores/m3). The drops of max-
imum daily concentration were recorded in the per-
iod from August to February, and December was the
month with the least maximum daily concentration
(17 spores/m3; Figure 1). April was the month with
the highest mean daily concentration (28 spores/m3)
and January was the month with the lowest mean
daily concentration (7 spores/m3). The lowest value
of minimum daily concentration of spores was
recorded in February (1 spore/m3), while the max-
imum value of minimum daily concentration was
recorded in August (9 spores/m3; Figure 1). The
daily concentrations of the most common genus
Cladosporium were contrasted the total fungal spores
during the year of study (Figure 2). Variations in
daily concentrations alternated between species that
have average daily concentrations of 0.28 to 1.72
spores/m3 of air (Figure 3) and lower concentrations
of 0.13 to 0.28 spores/m3 of air (Figure 4).
Diversity and seasonal variation of airborne fungal spores
According to the fungal diversity, February–April
were the months with the highest diversity with a
record of 39 out of 41 genera (Table I). A clear
and gradual decreasing in fungal diversity was
obtained from June to November 2009. A gradual
increase was obtained in December 2008 and up to
February 2009 (Table I).
Deuteromycota was the highest in number in the
whole year with two peaks, one in June (7749 spores/
m3) and another one in April (7613 spores/m3).
Basidiomycota was the next in abundance with
almost similar trends in seasonal fluctuation and
two peaks, one in April (3481 spores/m3) and
another one in July (3257 spores/m3). Ascomycota
is relatively low in number with a little fluctuation
and two short peaks, one in January (550 spores/m3)
and another one in April (718 spores/m3).
Zygomycota was the least in number in relation to
other taxa with the highest number obtained in April
(90 spores/m3) and the lowest with zero value
obtained in August (Figure 5).
Fungal spores and meteorological factors
Correlation analysis was carried out between daily
meteorological data and total daily counts as well as
between daily meteorological data and daily counts of
the most abundant genera (Alternaria, Cladosporium,
Drechslera, Puccinia, Ustilago) recorded in the atmo-
sphere of Zarqa area (Table II). Total daily spore
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Table I. Monthly and annual counts of fungal spores trapped during the study year (December 2008–November 2009) from the atmosphere of the Zarqa area, Jordan.
120

Genus name Dec 08 Jan 09 Feb 09 Mar 09 Apr 09 May 09 Jun 09 Jul 09 Aug 09 Sep 09 Oct 09 Nov 09 Total per year % of Total

Agaricus 25 17 47 11 21 17 0 0 0 0 4 15 157 0.21

Alternaria 501 219 139 201 723 652 825 1055 539 360 337 328 5879 7.70
Aspergillus/Penicillium 25 296 108 169 231 89 135 80 116 50 47 58 1404 1.84
Beltrania 2 0 5 44 43 48 58 22 4 13 1 1 241 0.32
Bispora 22 18 12 13 10 10 4 5 0 0 0 0 94 0.12
Botrytis 110 87 101 131 251 75 112 103 64 46 31 93 1204 1.58
Bulgaria 34 24 50 19 51 31 42 52 24 20 16 140 503 0.66
Chaetomium 137 85 49 58 100 107 90 67 61 117 77 21 969 1.27
Cladosporium 2312 1171 1491 1811 4732 3696 5596 4654 3652 3129 2079 3411 37734 49.39
Cochliobolus 22 13 16 17 67 40 25 20 14 13 11 5 263 0.34
Coprinus 0 5 21 5 33 5 26 5 2 6 7 18 133 0.17
Deightoniella 9 3 8 6 0 1 0 0 0 0 0 0 27 0.04
Diplococcium 9 19 9 13 4 6 9 1 5 0 1 0 76 0.10
Drechslera 111 70 101 224 803 504 359 402 173 130 132 72 3081 4.03
M. H. Abu-Dieyeh and R. Barham

Epicoccum 12 55 46 65 60 102 48 36 34 35 21 29 543 0.71

Erysiphe 0 12 33 41 81 72 41 53 31 11 22 0 397 0.52
Fusarium 32 39 29 63 167 77 52 38 28 9 25 6 565 0.74
Ganoderma 4 4 2 8 9 9 16 22 21 58 27 17 197 0.26
Humicola 14 27 18 14 26 14 64 26 19 14 26 19 281 0.37
Leptosphaeria 68 48 18 77 72 42 90 48 37 33 54 21 608 0.80
Melanomma 62 53 39 36 88 15 26 15 10 46 14 13 417 0.55
Melanospora 22 3 3 5 6 37 19 13 7 0 3 2 120 0.16
Nectria 5 9 12 2 10 0 0 0 0 0 0 0 38 0.05
Nigrospora 0 8 11 20 15 23 6 8 9 8 0 0 108 0.14
Paecilomyces 59 48 55 90 17 23 71 57 28 27 35 30 540 0.71
Papularia 12 19 23 112 315 37 151 41 7 0 2 0 719 0.94
Phragmedium 0 0 0 0 8 10 19 6 3 0 0 0 46 0.06
Pleospora 5 3 7 8 3 6 8 5 1 1 6 7 60 0.08
Puccinia Teliospores 0 13 8 6 25 18 29 20 10 0 0 0 129 0.17
Puccinia Uredospores 230 190 198 290 334 681 1314 2766 1186 959 223 143 8514 11.14
Rhizopus 19 45 77 34 90 47 78 3 0 12 12 20 437 0.57
Sordaria 10 3 11 16 6 10 17 8 2 0 0 0 83 0.11
Spegazzinia 0 0 0 1 3 4 4 0 0 1 0 0 13 0.02
Stemphylium 82 91 104 164 180 110 137 68 66 29 50 42 1123 1.47
Tilletia 9 65 95 120 97 81 99 51 27 20 14 12 690 0.90
Torula 120 72 15 85 115 110 116 54 63 8 45 22 825 1.08
Tricocladium 4 2 3 19 13 4 4 0 7 2 0 1 59 0.08
Tricothothecium 13 12 10 0 0 0 0 0 0 0 0 0 35 0.05
Ulocladium 76 89 46 27 72 64 112 65 41 13 45 21 671 0.88
Ustilago 184 97 136 402 2954 716 560 387 200 83 88 17 5824 7.62
Venturia 39 14 17 37 67 34 29 37 12 2 10 7 305 0.40
Unknown 149 18 11 20 115 99 306 300 196 28 28 14 1284 1.68
Total 4549 3066 3184 4484 12017 7726 10697 10593 6699 5283 3493 4605 76396 100%
Number of fungal genera 35 38 39 39 39 39 37 35 34 30 31 29

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counts showed a significant positive correlation
(P ≤ 0.05) with maximum temperature and a signifi-
cant negative correlation (P ≤ 0.05) with relative
humidity. No significant correlations were obtained
between total daily spore count and other weather
parameters (Table II).
Drechslera and Ustilago are two common fungal
spores in the atmosphere of Zarqa; however, they
did not significantly correlate with the studied
weather parameters. Cladosporium showed a highly
significant positive correlation (P ≤ 0.01) with max-
imum temperature and a highly significant nega-
tive correlation with relative humidity (P ≤ 0.01).
Alternaria daily counts significantly and positively
correlated with maximum and minimum tempera-
ture and negatively correlated with both rainfall
and relative humidity. Puccinia uredospores
showed a little difference in correlation analysis
than other genera as they showed a positive sig-
nificant correlation with wind speed, maximum
temperature and minimum temperature, but no
significant correlations with relative humidity and
rainfall (Table II).
Diurnal variations of airborne fungal spores
No significant differences in mean monthly fungal
spore counts were obtained among the three peri-
ods from December 2008 to May 2009 (Figure 6).
However, significant differences in diurnal fluctua-
tions were observed from June to November 2009
Fungal airborne spores of Jordan (Zarqa) 121
Figure 1. Daily concentration of fungal
spores recorded in each month of the
study (December 2008–November 2009)
in the atmosphere of the Zarqa area,
Jordan. Dotted lines refer to the mean
daily count. Blacked circles represent the
outlier values.
with significantly greater fungal counts in the time
period from 20.00–04.00 compared to counts of
the other time periods (Figure 6). Alternaria,
Cladosporium, Drechslera and Puccinia showed sig-
nificant differences between the three periods; the
20.00–04.00 period had the greatest values of daily
spore counts (Table III). However, spores of
Ustilago showed no significant differences in daily
spore counts for the three periods (Table III).
Discussion
Annual counts and common airborne fungal spores in the
atmosphere of Zarqa
The Zarqa area is specifically classified as arid
Mediterranean with typically Irano-Turanian
(steppe) vegetation (Zohary 1962; Al-Eisawi 1985)
and located as ecotone between the Mediterranean
and Eastern desert vegetation. The Amman area is
classified as semi-arid Mediterranean (Al-Eisawi
1985) with about four-fold increase of the average
annual rainfall (400–500 mm) than Zarqa. This may
explain the six-fold increase in quantity of the total
annual aerospora (461 779 spores/m3) reported in
the Amman area by Shaheen (1992). In the present
study, Deuteromycota spores represent 72.3% fol-
lowed by Basidiomycota (20.6%), Ascomycota
(6.5%) and then Zygomycota (0.6%). A similar
order of aerospora taxa was observed in Amman
(Shaheen 1992). Generally deuteromycetes and
 122 M. H. Abu-Dieyeh and R. Barham
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basidiomycetes have wider ranges of dispersal than
ascomycetes (Gaur & Kala 1984).
Cladosporium was found to be the main constituent
of airborne fungal spores forming almost 50% of the
total aerospora (Figure 1, Table I). This result coin-
cides with what has been previously recorded about
the Zarqa area using the settle exposure method
(Abu-Dieyeh et al. 2010). Cladosporium was also
considered the main airborne constituent of the air
at Amman reaching 72.1% of the total trapped aero-
spora (Shaheen 1992). Coinciding with other studies
from different countries, Cladosporium was found to
be one of the most, if not the most, common aero-
spore (Lacey 1981; Shaheen 1992; El-Essawy et al.
1992; El-Said & Abdel-Hafez 1995; Al-Subai 2002;
Ismail et al. 2002; Asan et al. 2004; Hedayati et al.
2005; Oliveira et al. 2005; Özkara et al. 2007).
Shaheen (1992) explained the abundance of
Cladosporium in the atmosphere by the structural
features of their spores such as small size, thin
exine and smooth wall, which favour and facilitate
the transport of airborne spores. Other authors have
indicated that Cladosporium spores are the dominant
aerospora in hot climates (Takahashi 1997; Şen &
Asan 2001; Al-Subai 2002; El-Morsy 2006).
Cladosporium spores are identified as dark-coloured
spores; Al-Subai (2002) presented a good discussion
about the prevalence of dark coloured spores in hot
climate atmospheres since they are more resistant to
Figure 2. Daily spore concentrations dur-
ing the year of study (1 December 2008–30
November 2009) for total fungal spores
(A) and for the most common genus
Cladosporium (B) in the atmosphere of the
Zarqa area, Jordan.
desiccation (Nicot 1960; Ranzoni 1968; Moubashe
& Mazen 1972), strong light (Nicot 1960) and ultra-
violet radiation (Durrel & Shields 1960).
Cladosporium in addition to Puccinia uredospores,
Alternaria, Ustilago and Drechslera represent about
80% of the total trapped fungal spores in the air of
the Zarqa area (Table I). Alteranaria, in the present
study, has a similar quantity (7.7% of the total aero-
spora) to what has been reported by the settle expo-
sure method in Zarqa (Abu-Dieyeh et al. 2010);
however, the genera Puccinia, Ustilago and
Drechslera are biotrophic fungi, which do not grow
on culture media and, consequently, were not
recorded using the settle exposure method (Abu-
Dieyeh et al. 2010).
In contrast, a genus like Fusarium is known to be
better detected on settle exposure rather than spore
trapping (Mitakakis & Guest 2001); therefore, it was
reported in the present study as a rare constituent
(0.74% of total aerospora) (Table I), while it was one
of the most abundant (20%) of the total recovered
fungi using the settle exposure method (Abu-Dieyeh
et al. 2010). Fusarium species do not grow well at
low water activity level and usually colonise very
damp or wet materials. In addition, airborne micro-
conidia and chlamydospores of Fusarium are difficult
to identify in air samples analysed by direct micro-
scopy, hence, only the macroconidia of some species
may be detected (Nelson et al. 1994). Fusarium is
 Fungal airborne spores of Jordan (Zarqa) 123
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Figure 3. Daily spore concentrations during the year of study (1 December 2008–30 November 2009) for fungal spores that have an average
daily concentration of 0.28 to 1.72 spores/m3 of atmospheric air of Zarqa, Jordan.
 124 M. H. Abu-Dieyeh and R. Barham
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Figure 4. Daily spore concentrations during the year of study (1 December 2008–30 November 2009) for fungal spores that have an average
daily concentration of 0.13 to 0.28 spores/m3 of atmospheric air of Zarqa, Jordan.
 Fungal airborne spores of Jordan (Zarqa) 125

Figure 5. Fluctuation of major fungal spore

taxa collected from the atmosphere of the
Zarqa area, Jordan, during the year of
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study (December 2008–November 2009).

known as a pathogen for some cultivated plants and
also as allergenic fungus (Şen & Asan 2001).
The greatest rush of Cladosporium occurred in the
last ten days of March; however, it prevailed in high
quantities throughout the entire year (Figure 2). The
increase in number of Cladosporium was associated
with the accumulation of plant vegetative matter
(Moustafa & Kamel 1976), and/or climatic factors
(Stępalska & Wołek 2009). In Zarqa, using the settle
exposure method, Cladosporium was also the most
abundant peaking in March and November (Abu-
Dieyeh et al. 2010).
Altenaria, a fungus with larger spores, is known to
be responsible for causing an allergic respiratory
problem in humans as well as diseases in various
plants (Shaheen 1989). It represents the third most
common aerospora in the Zarqa area (7.7%). Spores
of Altenaria were recorded throughout the year; they
showed increases starting from the end of March till
the end of July. A little rush occurred in the begin-
ning of December (Figure 3). Alternaria was the only
genus that has been collected in similar percentages
of total aerospora of Zarqa from both methods, the
settle culture (Abu-Dieyeh et al. 2010) and the spore
trapping of the present study.
Puccinia is the second most abundant fungal spore
in the air of the Zarqa area with a percentage of
11.14% of total aerospora prevailing from June to
September (Figure 1). In the Amman area, the max-
imum uredospores incidence was reported between
July and August (Shaheen 1992). This is highly
related to the maximum seasonal growth of their
host plants encountered in the area (Gaur & Kala
1984; Shaheen 1992). This kind of spores is not
necessary to be locally presented in the area, but
they are transported over very long distances, even
between continents (Brown & Hovmoller 2002).
Therefore, Puccinia spores are expected to originate
from wheat agricultural plots located anywhere in
Jordan or even in border countries, mainly Syria.
The life cycle of Puccinia occurs in regular steps
throughout two periods: the infection of wheat by
aeciospores occurs at the end of spring and the con-
centration of uredospores increases in the summer.
This may explain their prevalence throughout May–
September. However, autumn wheat crops are

Table II. Correlation analysis (Pearson) between daily meteorological data and total daily spore counts in addition to daily count of the most
abundant genera recorded in the atmosphere of the Zarqa area, Jordan (December 2008–November 2009).

Alternaria Cladosporium Drechslera Puccinia (uredospores) Ustilago Total spore count

Max temp (°C) 0.711** 0.790 ** 0.317 0.699* 0.187 0.646*

Min temp (°C) 0.648* 0.681* 0.306 0.754** –0.0408 0.506
Mean temp (°C) 0.761* 0.722** 0.292 0.78** 0.195 0.69*
Rainfall (mm) –0.614* –0.550 –0.297 –0.427 –0.251 –0.539
Wind speed (km/h) 0.458 0.338 0.246 0.686* 0.168 0.453
Relative humidity (%) –0.725** –0.730 ** –0.102 –0.544 –0.341 –0.690*

*Refers to significant correlation at P ≤ 0.05

**Refers to significant correlation at P ≤ 0.01.
 126 M. H. Abu-Dieyeh and R. Barham

Figure 6. Diurnal variation of mean

monthly airborne fungal spore counts in
the Zarqa area, Jordan, throughout the
study period (December 2008–November
2009). Within each month, mean values
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with a common letter are not significantly

different according to a Tukey’s test at
P ≤ 0.05.

suspected to new fall infection, which allows patho- (0.27%) (Shaheen 1992). However, using the settled
gens to persist throughout the year (Brown & exposure method, they were collected in Zarqa in
Hovmoller 2002). higher percentages: 4.2% for Penicillium and 3.6%
Ustilago was the fourth most common fungal for Aspergillus (Abu-Dieyeh et al. 2010). Spores of
spores in the area, with a percentage of 7.62% of Penicillium and Aspergillus are 1–2 µm in aerodynamic
total aerospora (Figure 1). Ustilago mainly dominates diameter (Mitakakis & Guest 2001) and, according to
in April and May and decreases in quantity from Hirst (1952), the Burkard trap is unable to accurately
June to July (Figure 3) with a quantity resembling collect particles less than 5 μm in aerodynamic dia-
that obtained in the Amman area (7.44%; Shaheen meter. Fungi with small-spores of less than 5 μm in
1992). Favourable temperature and humidity as well diameter include Aspergillus, Penicillium, Botrytis,
as the presence of cereal crops may explain the high Paecilomyces, Phoma and Nigrospora. All of these are
incidence of Ustilago in spring months (Sabariego expected to be under-estimated in this study; there-
et al. 2000; Oliveira et al. 2005). fore, viable culture on open plate should be integrated
Drechslera was the fifth most common airborne with the spore trapping method. Mitakakis and
fungal spores in the Zarqa area with a percentage of Guest (2001) recommended the use of a viable volu-
4.03% of total aerospora (Table I). High incidence metric Andersen sampler along with the Burkard
of this fungus was obtained in April and May (Figure spore trap.
4). According to Yang and Heinsohn (2007), the Ganoderma is another fungal spore detected in the
release of Drechslera spores is mainly affected by present study with 0.26% of the total aerospora
decreasing relative humidity and not due to tempera- (Table I). This fungal spore is known as an allergen
ture changes. (Bush & Portnoy 2001). Its presence in low
Spores of Aspergillus and Penicillium are considered
relevant spores in aerobiology, because some species
are allergenic to humans. They also act as pathogens Table III. Diurnal variations of mean daily airborne fungal spore
for humans, animals and plants (Su et al. 1992). counts of the most abundant species recorded in the atmosphere of
Zarqa, Jordan (December 2008–November 2009).
Dark-coloured Aspergillus and Penicillium, especially
A. niger Tiegh., A. terreus Thom and P. funiculosum Time interval 12.00–20.00 20.00–04.00 04.00–12.00
Thom, are the strongest survivors of irradiation and
Alternaria 4.906b 7.387a 4.537b
can tolerate temperatures up to 47 °C (Ranzoni
Cladosporium 27.784b 50.983a 28.474b
1968). Aspergillus and Penicillium spores are the Drechslera 2.287b 3.980a 2.486b
most widespread aeroallergens in the world (Asan Puccinia 6.706b 10.700a 6.920b
et al. 2004). uredospores
In the present study, the Aspergillus/Penicillium Ustilago 4.311a 7.811a 4.529a
group represented 1.84% of the total aerospora Note: Within rows, mean values with a common letter are not
(Table I). In the Amman area, it was much lower significantly different according to a Tukey’s test at P ≤ 0.05.

percentages may be due to unfavourable climate
conditions in the area. High concentrations of
Ganoderma occur when temperatures are generally
in the range of 15 to 20 °C and relative humidity is
high, exceeding 70% (Hasnain et al. 2004). Other
important fungal spores are shown in Figure 4.
Concentrations and diversity of airborne fungal spores in
the atmosphere of Zarqa
From the present study, the mean daily concentra-
tion of fungal spores in the air of Zarqa ranged from
7 spores/m3 (January) to 28 spores/m3 (April;
Figure 1). These values are much lower than what
was reported for airborne fungal spores in the
Amman area (15 spores/m3 in November 1987,
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and 267 spores/m3 in October 1987; Shaheen
1992). Vegetation density and diversity are the
major contributors of fungal spores (Gregory
1973; Moubasher 1993). High incidence of fungal
spores was reported over crops (Frinking 1991;
Brown & Hovmoller 2002). The arid environment
of Zarqa with much lower rainfall and humidity
levels offers very poor vegetation compared to that
of the Amman area, which, in consequence, leads
to a poor environment for fungal growth. Moreover,
the climax of vegetation in natural areas of Zarqa is
mainly bushes and sometimes shrubs. The only
short trees available are usually planted either as
crops (mainly olive) or ornamental trees (mainly
conifers). The vegetation in the Amman area is
dominated by typical Mediterranean vegetation
with a forest climax of Pinus, Quercus and others
(Al-Eisawi 1985). Moreover, agricultural plots and
ornamental plantings are much larger in Amman
than in Zarqa area.
Our results of mean and maximum daily concen-
trations of fungal spores showed two peaks (April
and June); the lowest concentrations were recorded
in the winter season (December–February; Figure
1). Generally speaking, in spring, conidiospores
and teliospores are predominant in the air, which
might be due to favourable temperature and humid-
ity conditions, while the decrease in spores in winter
might be due to the low temperatures, which have a
negative effect on the content spore particles in the
air (Sabariego et al. 2000). Results from the settle
exposure method in Zarqa showed two peaks
(March and November–December; Abu-Dieyeh
et al. 2010). In the Amman area, Shaheen (1992)
found that a multi-peak system with October as the
month of highest fungal spore count and no peak in
winter months (November–March). In dry and
desert environments in Kuwait, similar to the
Zarqa climatic pattern, the monthly total number
Fungal airborne spores of Jordan (Zarqa) 127
of fungi showed remarkable seasonal periodicity
with the greatest number of colonies occurring in
March–April and November (Moustafa & Kamel
1976); in Qatar, the two peaks were recognised in
July and December (Al-Subai 2002); in Assiut,
Egypt, the peaks occurred in spring and autumn
and the trough in summer (Moubasher & Moustafa
1974; Abdel-Hafez et al. 1993). The discrepancy in
seasonality of fungal spore count between similar
climate areas could be attributed to variations in
the local atmospheric conditions, vegetation density
and diversity, type of soil and climatic conditions.
Nevertheless, culture methods revealed only a por-
tion of airborne microorganisms, because some
fungi cannot grow at all on culture media and
some of them might be under-estimated or loose
viability due to competition from other fungi
(Mitakakis & Guest 2001; Pyrri & Kapsanaki-Gotsi
2007). Not only that, but also differences in sam-
pling height (Khattab & Levetin 2008), sampling
year and number of sampling days can change the
results between viable (culture method) and non-
viable (spore trapping) methods and make data
incomparable.
The Deuteromycota peak in April can easily be
explained due to the favourable conditions and
increased vegetation cover encountered in March;
however, most Deuteromycota are also considered
dry spores, which prevailed in low humidity condi-
tions (Moubasher & Al-Subai 1987). This may
explain their flourishing in June. Shaheen (1989)
attributed the seasonal periodicity of Basidiomycota
in Amman to the availability of the substrates
needed for fungal growth. No clear periodicity was
obtained for Ascomycota and Zygomycota
(Figure 5).
In addition to the ‘unknown’ group, 41 fungal
genera were recorded in the present study, whereof
the greatest number was trapped in February–April
(39 genera) and the lowest were in September–
November (29–31 genera; Table I). Magyar et al.
(2009) approved that positive correlations were
found between Simpson’s biodiversity index and
precipitation. March also was the month of highest
fungal diversity using the culture method accom-
plished in the Zarqa area (Abu-Dieyeh et al. 2010)
considering about 25 genera of fungi. This is easily
explained as it comes after the two months of the
highest rainfall and moderate temperature, January
and February, so the soil is moistened enough and
the vegetation is in its maximum growth and diver-
sity. Basically, soil and vegetation are considered the
main sources contributed for airborne fungal spores
(Moustafa 1971; Gregory 1973; Abdel-Gawad 1984;
Moubasher & Al-Subai 1987).
 128 M. H. Abu-Dieyeh and R. Barham

Correlations between spore counts and meteorological areas in different parts of the world (Levetin 1991;
factors Hasnain 1993; Li & Kendrick 1994; Grinn-Gofroń
et al. 2011). Wheat stem rust caused by Puccinia can
The significant effect of meteorological factors on
be dispersed hundreds or thousands of kilometres to
fungal spore counts is well documented in the lit-
the main wheat belt, and its dispersal is strongly
erature (Agarwal et al. 1969; Bandyopadhyay et al.
affected by wind speed (Aylor 1999; Brown &
1991; Hasnain 1993; Di Giorgio et al. 1996;
Hovmoller 2002).
Angulo et al. 1999; Sabariego et al. 2000; Al-
Our results showed positive correlations between
Subai 2002; Asan et al. 2004). Conversely, it is
minimum temperature and daily counts of
difficult to separate the individual effects of differ-
Alternaria, Cladosporium and Puccinia (Table II).
ent meteorological parameters, since fungi react
The hot climate during summer might explain the
simultaneously to a combination of factors (Azco
correlation between the earlier mentioned genera
& Talo 2000).
and minimum temperature. Grinn-Gofroń (2011)
Correlation analysis between daily meteorological
considered minimum temperature as the most
data and total daily spore counts showed significant
important meteorological factor associated with
positive correlations (P ≤ 0.05) with maximum and
spore types, especially in summer, in which the
mean temperatures and a significant negative corre-
strongest correlation was for Cladosporium and
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lation (P ≤ 0.05) with relative humidity (Table II).

Alternaria. An increase in Cladosporium spore level
Members of the dry aerospora are found in greatest
at minimum temperature above 13 °C during sum-
abundance in the atmosphere with conditions of
mer was also observed by Fernández et al. (1998)
low humidity and high wind speeds (Levetin 1991).
and Stępalska and Wołek (2005).
In the Zarqa area, the vegetation and mainly the
Alternaria was the only fungal genus that showed a
annuals flourish during January and March.
negative correlation with rainfall (Table II). The
Therefore, the first peak of total spore count was in
rainy months (October–March) of the Zarqa area
April following the two months with the highest rain-
matches the months of lowest concentrations of
fall and most moderate temperatures. Similar trends
total aerospora. Similarly, rainfall caused a pro-
occurred in the Amman area (Shaheen 1989) as low
nounced decrease in fungal spore counts in the
relative humidity and high temperature favoured
Amman area (Shaheen 1989). From other studies,
spore liberation and correlated with high spore
correlations with rainfall were found to be variable
count. Clearly, the June–July peak in total spore
and apparently they are affected by the nature of the
count can be explained as a kind of rush for dry
species and interacted with other weather conditions.
spores of i.e. Cladosporium, Alternaria and Puccinia,
Rainfall was negatively correlated with concentra-
which clearly dominated the air of Zarqa.
tions of most dry spores except for Cladosporium
Cladosporium and Alternaria both showed highly sig-
and Botrytis (Stępalska & Wołek 2005). Conversely,
nificant positive correlations (P ≤ 0.01) with maxi-
Mitakakis et al. (1997) reported a negative correla-
mum and mean temperatures and highly significant
tion with rainfall for Cladosporium. Generally speak-
negative correlations with relative humidity
ing, rainfall can cause reduction in airborne fungal
(P ≤ 0.01). This correlation might explain the shift
spore count in two ways: by washing off fungal
of the first peak to a less humid month, April, and
spores as well as other particulate matter (Shaheen
also explain the presence of the second peak in a hot
1989) and/or by wetting the surface of vegetation
and dry month, June. Many authors found a strong
temporarily and, in consequence, inhibiting spore
association or correlation between average daily tem-
dissemination (Davies 1969). However, ascospores
peratures and average daily counts of Cladosporium
and spores of Fusarium were found to flourish and
and Alternaria (Katial et al. 1997; Troutt & Levetin
increase in the atmosphere due to precipitation
2001; Stępalska & Wołek 2005) as well as a negative
(Burge 1986; Shaheen 1989). Burge (1986) men-
correlation between both genera and relative humid-
tioned that, some ascospore types require active pre-
ity (Grinn-Gofroń & Mika 2008).
cipitation for dispersal.
Puccinia showed positive significant correlations
Drechslera and Ustilago are two common fungal
with wind speed, maximum, mean and minimum
spores in the atmosphere of the Zarqa area, but
temperatures and no significant correlations with
they did not significantly correlate with meteoro-
relative humidity and rainfall (Table II). The positive
logical factors. This is likely, because the concen-
correlation with maximum temperature can explain
trations of these genera were mainly limited to
the high number of Puccinia uredospores recorded in
certain months (March–July) and the gaps in
July. Basidiospores can be dispersed over long dis-
daily data making them not suitable for correlation
tances by wind; they also have been considered as an
analysis.
important component of the aerospora in urban
 Fungal airborne spores of Jordan (Zarqa) 129

Diurnal fluctuation of airborne fungal spores From the present study, the common fungal
spores, Cladosporium, Alternaria, Puccinia uredospores
Among the studied periods (12.00–20.00, 20.00–
and Drechslera are all favoured by the midnight and
04.00 and 04.00–12.00), significant differences in
early morning period (20.00–04.00; Table III).
mean monthly spore counts occurred from June to
Decreasing the relative humidity in the morning is
November 2009, in which the fungal spore release
the reason for the presence of many spores in the air
favoured midnight to early morning (20.00–04.00)
(Hirst 1959). Concerning Cladosporium, reports from
over the other two periods (Figure 6).
other studies shows the maximum concentration of
Our findings of the greatest release of fungal
spores occurred at about noon (Stępalska & Wołek
spores during the intradiuranal period from mid-
2009), between 12.00–14.00 (Rantio-Lehtimäki
night to early morning coincide with results from
et al. 1991), 14.00–15.00 (Burge 1986), 15.00–
other studies (Rosas et al. 1993; Ho et al. 2005;
16.00 (Adams 1964) and 20.00–22.00 (Media-Villa
Wu et al. 2007; Grinn-Gofroń 2011). Temperature
et al. 1997). For Alternaria, the maximum concen-
and dew point seemed to be the most important
trations were also reported in different intradiurnal
meteorological factors affecting airborne spore con-
periods: between 13.00–14.00 (Stępalska & Wołek
centrations (Troutt & Levetin 2001; Grinn-Gofroń
2009), 20.00–22.00 (Stach 1997), in the evening
2011). Many authors assumed that the intradiurnal
hours at about 20.00 (Corden & Millington 2001)
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rhythm, in which the highest abundance of spores is

and in early morning at about 08.00 (Hjelmroos
present between the midnight and early morning
1993). Spores of Cladosporium and Alternaria are
period, suggests an active release mechanism
dry spores and favoured the release into the atmo-
induced by the high dew point at dawn (Rosas
sphere under warm and dry conditions (Stępalska,
et al. 1993; Ho et al. 2005; Wu et al. 2007; Grinn-
Wołek 2009). The different results in the diurnal
Gofroń 2011). During summer and in hot areas, the
distribution of fungal spores can be explained by
minimum temperature is favoured by most spore
differences in weather conditions due to local, regio-
types, especially the dry spores, and it was consid-
nal and seasonal factors. However, specialists agreed
ered as the most important meteorological factor
that dry spores like Cladosporium and Alternaria need
associated with spore release (Grinn-Gofroń 2011).
relatively dry conditions to facilitate the discharge of
In addition to that, the spore release of some fungal
spores and conidia from the hyphae (Stępalska &
species is greatly affected by relative humidity
Wołek 2009). Therefore, the period of maximum
(Stępalska & Wołek 2005). During the study
concentration will be any intradiurnal period that
year, high temperature and low humidity were pre-
matches these conditions, in other words, the period
vailing from June to October in the Zarqa area
can range from midnight to early morning as long as
and, as previously mentioned, an abundance of
the weather is hot as in the present study, or around
Cladosporium, Alternaria and Puccinia correlated
evening similar to that reported in many European
with minimum temperature (Table II). However,
countries (Rantio-Lehtimäki et al. 1991; Stępalska &
very hot temperature during the day may play a
Wołek 2009).
significant role on decreasing spore release into the
Our results also indicated that uredospores of
air. The significant positive correlations between
Puccinia were found in maximum concentrations
temperatures and high levels of ozone in the atmo-
during the period from midnight to early morning.
sphere (Adhikari et al. 2006) may kill microorgan-
Spores of Basidiomycetes are released whenever they
isms by the oxidation of cellular components such as
become mature enough (Stępalska & Wołek 2009).
sulphydryl groups and amino acids of enzymes, pep-
In support of our findings, Breitenbach et al. (2002)
tides, proteins as well as through the oxidation of the
indicated that basidiospores usually show a strong
cell membrane (Daş et al. 2006).
diurnal rhythm with peak concentrations during
Contrary to our results, Giner et al. (2001)
late night to early morning hours. Other factors
recorded the lowest counts of fungal spores in the
may interact in the process of spore release and can
morning (at about 08.00), and, along with others
affect their concentrations in the atmosphere, among
(Ricci et al. 1995; Angulo et al. 1999; Rodríguez-
those the state of the host and the weathering on the
Rajo et al. 2005), recorded higher concentrations of
host plant as well as maturing and the kind of vege-
fungal spores in late evening period (19.00–22.00).
tation and local crops (Grinn-Gofroń & Mika 2008).
Giner et al. (2001) suggested that the late afternoon
maximum may be linked to a real late afternoon
release of conidia from local sources or to a delay
Acknowledgements
in the capture of spores released earlier and trans-
ported to the sampler from rural areas (15–30 km The authors are grateful for the financial support
away). provided by Faculty of Graduate Studies and
 130 M. H. Abu-Dieyeh and R. Barham
Scientific Research, The Hashemite University,
Zarqa, Jordan.
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