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Sistema de Información Científica
Red de Revistas Científicas de América Latina y el Caribe, España y Portugal
Contam. Ambient. 2, 13-23, 1986
AIRBORNE FUNGI ISOLATED FROM RAIN WATER
COLLECTED IN MEXICO CITY
IRMA ROSAS, CARMEN
CALDERON, SARA
GUTIERREZ
AND
PEDRO MOSIRO
Departamento de Química Atmosférica y Estudios
del Agua, Centro de Ciencias de la Atmósfera,
UNAM, Coyoacán, 04510, México, D. F.
RESUMEN
Se llevó a cabo una investigación sobre los hongos presentes cn la atmósfera de la
Ciudad de México, a través del análisis del agua dc lluvia colectada durante los meses
de junio a septiembre de 1982. Para lograr el aislamiento de una amplia gama de
hongos se utilizaron los medios de Sabouraud dextrosa agar y papa dextrosa agar,
incubados a temperatura ambiente (20-26vC) por 48-72 h. Durante cl muestre0 se
registraron entre 600 y 6000 colonias por ml. Los hongos que aparecieron con más
frecuencia fueron
Cladosporium, Alternaria, Penicillium
y levaduras. Se estableció la
relación que existe entre la abundancia de estos organismos e11 cl airc y los factores
ambientales.
Se observó que la velocidad del viento cstuvo relacionada con la abundancia de los
hongos en el agua de lluvia con una
r
de 0.80 (p
<
0.01). La identificación de algu-
nas colonias a nivel de especie, tales como
Penicillium citrinum,
P.
clauigerurn, Fusarium
semitectum, Asfiergillus niger, A. candidus, A. glaucus
y
A. tarnarii,
permitió señalar
la presencia de hongos patógenos o alergenos.
Esta información puede servir de base para estudios futuros sobre la implicación de
los factores ambientalcs en la abundancia y dispersión dc hongos importantes para los
sectores médico y agrícola.
ABSTRACT
A rcsearch was carried out on the lungi present in tlir atmosphere of Mexico City,
through the analysis of rain watcr collected from June to Septcmber of 1982. To obtain
data ori a wide range oí fungi, isolations were made on Sabouraud dextrosc agar and
potatc) dcxtrosc agar plates incubated at the rnom tcmperaturc of
20-26QC for 48-
72 hours.
During tlic sampling period 600 to GOOO colonies per m1 were rccorded. The most
frequent fungi were
Cladosporium, Alternaria, Penicillium
and yeasts. The relationship
between these airborne organisms and weather elements was established.
It was found that wind speed was related to fungal counts through a corrclation
coefficient of r
=
0.80 (p
<
0.01). Identification at thc species leve1 of some fungi,
such as
Penicillium citrinum, P. clavigerurn, Fusarium semitectum, Aspergillus niger,
A. candidus, A. glaucus
and
A. tamarii,
allowed to show the presence of both patho-
genic and allergenic fungi.
This infonnation could be used in further studies of
a
medical or agronomical char-
acter about. the effect of environmental factors on the abundance and dispersion of
airborne fungi.
INTRODUCTION
It has been shown by several research papers that the atmosphere bears microor-
ganisms which are able to survive in this adverse, gaseous environment for a con-
siderable lenght of time (Schlichting 1969, Edmons 1979, Jones and Cookson 1983,
Imshenetskii et
al.
1984). Among these microorganisms, about 1 200 species of
both bacteria and actinomycetes have been identified, moR than 100 000 different
types of pollen graim, and abundant spores from aproximately 40 000 species of
fungi, many mosses, liverworts and ferns (Gregoty 1973).
A great diversity of fungi has been isolated from the atmosphei~ elther through
direct sampling of the air or by the collecting of rain water (Overeem 1937, Gre-
gory
et al.
1955, Pady 1957, Maguire 1963, Goodman
et al.
1966). Gregory (1960)
suggests that an efficient method for the sampling of microorganisms present in
the air is to collect water and culture it on certain agar media. Thus a great amount
of algae, protozoa and fungal spores have been kollated from samples of rain water
(Schlichting 1961, Davies 1961, Mc Donald 1962, Maguire 1963, Starr and Masson
1066).
It is interesting to know the identit~
and amount of the fungal spores, because
they may produce disease in man and plants, as some of them have been reported
as phytopathogenic (Nutman
et al.
1960, Vander Plank 1967), and
as
producers
of mycotoxins which may contaminate food and storaged products (Moreno 1977,
Horsfall and Cowling 1978). Also, it has been reported that diverse fungi are
pathogenic for both animals and man (Jungerman and Schwarts 1972, Rippon
1974, Alexopoulos and Mims 1979). The inhalation of these
type
of microorganisms
may induce allergenic reactions in man, so the cxposure to high concentractians of
them implies a risk to health (Myde
et al.
1956, Sandhu
et al.
1964).
To acquire a knowledge of the behaviour of fungal spores in the atmosphere, it
is not enough to obtain information on its biology, but also it is necesasary to generate
information on the environmental factors that affect both their release and distri-
bution (Rich and Waggoner 1962). In the present paper it was considered impor-
tant to isolate the fungi present in rain water, as a first stage in the research of
the airborne mycoflora of Mexico City.
MATERIALS AND METHODS
The sampling site is at the Center of Atmospheric Scknces in the campus of the
National Univenity of Mexico, located southewest of downtown Mexico City.
The Federal District plus its surroundings .represent a population of ahout 17
X
10"
inhabitants, iii 3.1
X
100 habitational units, 130
000
factorics and 3
X
100 veliicles.
The valley in which Mexico City
is
located is considered one of the most conta-
minated areas of the world.
The rain water samples were collected by means of a sampler, which consisted
of an iron
bars
frame,
2
m in height which supports a funnel of 28 cm in diameter
seated on an sterilized E~lenmeyer
flask (Maguire 1963). The funnel was covered
with aluminium foil up to
the
moment the rain started.
For isolating the fungi from rain water samples, a medium of
potato
dextrose
agar (PDA) with streptomycin was
used.
The rain water
was
subjected to dilutions
of 0.1, 0.01 and 0.001. With these subsampks thc culture medium was inoculated
AIRBORNE FUNGI IN RAIN WATER
and incubated for 3 days at room tempcrature; afteiwards, thc colonies tliat deve-
loped different characteristics were counted and transfered to new Petri dishes
containing sterile Sabouraud dextrose agar to identify the developed fungal cultures.
To obsem the fungal structures under the microscope, microcultures \vere made
which were fixed and stained with lactophenol cotton blue. To furtlier identify the
fimgi at the genus level the following works were consulted
:
Fitzpatrick
(
1930),
Raper and Fennel (1965), and Barnet and Hunter (1972). In some cases the iden-
tification was made at the species level using the books of Raper and Fennel (1965)
and of Pitt (1985).
RESULTS
Twenty three samples of rain water obtained from the Mexico City ama were
taken, and a total of 23 genera of fungi were identified belonging to the classes
Blastomycetes, Hyphomycetes, Coelomycetes and Zygomycetes. Thc fungi ,most fre-
quently found during the sampling period were species of
Clado.cpor,iicm, Alternaria
and
Penicillium,
as well as yeasts (Table 1). Thc iclentification of some fungal
colonies at the species level was done, including the following:
P~nicillum
citrinunl
Thom,
P. clavigerum
Demelius,
Fusarium semitrctiim
Berk
&
Rav.,
Aspergillus
niger
van Tiegh.,
A. candidus
Link,
A. flavus
Link,
A. glcucus
Link, and
A. tamar.'i
Kita. From Fig. 1 it can be deduced that in the rainy months (from June through
September) tlie most abundant fungi were
Cladosporc'urn
and yeasts. The numbers
obtained show that the heavy rainfall of Jiine carry few fungal spores, whereas
the August rains contain great amounts of fungal spores, in spite of the lesser rain-
fall recorded in this month (Table 11). It is important to point out tliat liourly
counts of fungi show two peaks related to the starting time of rain, one at 12: 30
and another at 16:30; the former peak is the larger one (Fig.
2).
Weather ele-
AL1ERNAII.A
M
ASPEROILLUS
m
CLAOOSPOR UH
1
:usARRtUU
m
CENlClLLlUY
mmp
rrrsrs
JUNE
JULY
AUGUST
SEPTEMBER
FIG.
1.
Fungi isolated from rain water collcctcd at the Univcrsity of Mexico City.
TABLE 1. PERCENT FREQUENCY OF OCURRENCE OF FUNGI
ISOLATED 'FROM RAIN WATER COLLECTED
AT THE UNIVERSITY OF MEXICO
Taxa
Frequency
CLASS 1-IYPHOMYCETES
Alternarra
Aspergillus
Botrytis
Chalara
Cladosporium
Epicocumm
Fusarium
Geotr.
.chum
Gonotr;ichum
Monilia
Penicillium
Pyricularia
Phynchosporium
Scopulariopsis
Trichoderma
Verticiillium
CLASS COELOMYCETES
Astermella
Chaetophoma
Dothiorella
PAoma
Peyronellaea
Phyllosticta
CLASS ZYGOMYCETLS
Rhizopzls
CLASS BLASTOMYCETES
Yeasts
(
unidentified
)
mrnts recorded during the sarnpling periods are shown in Table 111. As
to
tem-
perature and relative humidity, these ranged from 13.99 to
19QC
and 53.2
to
78.2%,
rcspectively.
AIRBORNE FUNOI IN RAIN WATER
TABLE 11. FUNGAL COUNTS FROM RAIN SAMPLE
AT THE UNIVERSITY OF MEXICO CITY
Date
Colonics/ml
Rainfdl mm
Ruin starting time
JUNE
14
23
29
30
JULY
02
12
27
AUGUST
02
03
09
1 o
11
12
16
18
19
24
25
SEPTEMBER
08
13
20
2 1
22
The sultriness index was low in general, its values ranging between
116.3
and
302.7
mb C . The winds were light and from the NE. In correlating further fungal
counts with the weather parameters above mentioned, it was found that a rela-
tionship exists with wind speed r
=
0.81
(p
<
0.01).
However, the correlation
coefficients for temperature and relative humidity were low (Table IV). The sul-
triness index and the rainfall show a good relationship with r
=
0.40
(p
<
0.05).
Fig. 3
shm
that the highest counts were obtained with the highest recorded
wind speeds, mostly with a northerly wind. However, it must be pointed out that
the lighter winds were the most frequent.
STARTARTING TIME OF
RAIN (hrs)
FIG. 2. Relationship betwaen fungal colonies in rain water and starting time of the rain.
DISCUSSION
Through the mycological analysis of rain water, several types of fungi were found
in the atrnosphere of Mexico City. The atmospheric washout that rainfall exerts is
able of removing spores and other fragments of fungi. It was also observed that
some environmental factors exert an influence on the concentration of these mi-
croorganisms in the air. The measure of the abundance of isolated fungi is referred
to as colonies per ml, regardless of the quantity of spores suspended in the air, since
it has been proved that hyphal fragments are present in the air and that they are
able to develop into colonies (Pady and Kramer 1960).
Research done in different parts of the world on some qualitative aspects of
airborne fungi, rhow that there are basic groups of fungi of universal distribution
(Ha~ris
1950, Dye and Vernon 1952, Morrow
et al.
1964, Ogunlana 1975). Most
of the isolated fungi reported in the present paper fa11 within such a group.
The 23 genera isolated through the 23 sarnplings belong to the airborne fungi
more commonly found in tropical areas (Kramer
et al.
1963, Goodman
et
al.
1966). Among the fungi more frequently isolated are specIes of
Claldosporj.um,
Alternaria, EusaRum, Penicillium
and
Aspergillur,
as w ll
as
unidentified yeasts.
The first genus was the most abundant.
Pady et
al.
(1962) and Rich and Waggoner (1962) report
Clados~orium
as
one of the most common fungi found in the air, which is probably due to its high
resistance to atmospheric cond.itions (Pady 1957). It has also been observed that
there are environmental factors that determine both the release of spores and their
introduction in the atrnosphere, to the extent that being a soil fungus it is more
frequently found in the air (Gregory 1973). The amount of
Cladosporium
re-
corded could be due to the fact that the Universit~
campus
is
surrounded by green
areas which provide adequate substrata for colonization; Richards (1956) and
Davies
e:
al. (1963) refer to it as an open field fungus. Not so for
Penicillium
AIRBORNE
FUNGI
IN RAIN WATER
which was less abundant during the sampling periods, confirming that it
i^r
a fungal
species characteristic of urban areas and common in home dust (Davies
1960).
Alternaria
and
Fusmium
were also present but never in great amounts. Despite
the determinations were made in rain water samples and not referred to as count-
ings
per
cubic meter, it
was
posible to detect some relationships between abudance
and the weather conditions.
TABLE 111. WEATHER CONDITIONS AT THE UNIVERSITY
OF MEXICO DURING THE SAMPLING TIME
Air
Tempera-
Relative
Sultriness
Wind
Date
ture
'C
Humidityyo
Zndex mb
"C
Direction
Sfieed m/s
JUNE
14
23
29
30
JULY
02
12
2 7
AUGUST
02
03
09
10
11
12
16
18
19
24
25
N-NE
SE
N-NE
S-SW
E-NE
NE
N-NE
SEPTEMBER
08
16.1
64.1
302.7
NW
1
.O
13
16.9
65.6
160.5
W
0.9
20
15.3
60.6
116.3
NW
2.0
2 1
16.7
53.9
130.8
N
1.5
22
15.9
68.3
152.6
NE
0.8
Regarding thc influence that rain exerts on the fungal content of the atmosphere
there exist several opinions.'It is important to point out that most of the data refer
to
Cladosporium,
and considering that in the present study it was the most abun-
dant, this information may be interesting to discuss. The results show that there
is a good inverse relationship between the fungal concentration and the rainfall
amount, indicating that the light rains bring down a larger amount of spores than
the heavy ones (Mc Donaild 1962, Rich
and
Waggoner 1962).
On relating the fungal content to the starting hour of the rain a double peak
was observed coinciding this with the known behaviour of
Cladosporium
during
the hours of light. It is considered that the first peak coincides with the start of
mechanical turbulence; with thk spores reaching gmat heights between 13
:O0
and
15:OO hours, so that spore amolints dilute into a larger volume of ai,r by thermal
turbulence, giving low counts in the sarnples of rain water within that lapse of time.
The second peak coincides with the reduction of thermal turbulence that permits
the descent of the spores down to the collectors's height. Si,milar findings have
been reported by Cammack (1955) and Rich and Waggoner (1962).
Among the most frequently isolated fungi thme were those with dry spores, for
which there is no mechanism for their active release, responsible for the introduc-
tion of these fungi into the air, but environmental factors such as strong wind,
thermals and the splashing up of the rain may be
the
only factors responsible for
both the release and dispersion of this kind of fungi in the atmosphere. There are
some data on the fluctuation of the quantity of spores because of weather elements
(Hirst 1953, Hamilton 1957, Zoberi 1964, Gregory 1973).
TABLE IV. CORRELATION COEFFICIENTS BETWEEN FUNGAL
COUNTS AND WEATHER
DEPENDENT VARIABLE
INDEPENDENT VARIABLE
.Pearson's correlation coeficcient
Fungal colonies/ml
Relative humidi ty
Temperature
Sultriness index
Wind speed
Rainfall
Tlie present paper shows that wind speed influenced the spore concentration in
rain water. It was observed that fungal spore counts increased as wind speed also
increased, and that during the sampling hours pmvailed the winds from the north;
the winds from the south had little influence because of their low velocity, coin-
ciding with the data of Kramer et
al.
(
1963))
and Hammet
and
Manners (1971).
AIRBORNE PUNGI IN RAIN WATER
Together with the above it can be pointed out that fungi are
a
prominent com-
ponent of aerial biota and it is vei)r irnportant to generate both qualitative and
quantitative information through both the diurna1 and seasonal variation of these
rnicroorganisms in the atmosphere of Mexico City. It is believed that the informa-
tion obtained on airbome fungi brought down by rainwater can serve as a base
for the future evaluation of the relationships between the weather and the myco-
logy of the air.
Among the fungi identified at the species level, some of them are known to be
pathogenic to human and/or animals, such as
Aspergillus flavus, A. niger
and
Penicillum citrinum
(Emmons
et al.
1970),
and as phytopathogenic
Aspergillus
candidus, A. flavus, A. niger,
and
Fusarium semitectum
(Moreno
1977).
ACKNOWLEDCMENTS
loow
1000
amo
400
f-
Y
;*o,
O
A
(.
I
L
iwo
DO0
-00
The authors are grateful to Guadalupe Rq-Ocotla, Alma Yela and Vida1 Val-
derrama for their assistance and to Dr. Miguel Ulloa and Mario Cruz for the
review of the manuscript and his valuable comments.
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WlIlO =LO
-A
FIG.
3. Relationship between fungal colonies and wind speed. (Arrows show wind direction).
i
-
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5
<\
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,,
x\
\
/
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400-~1~lfi~~~~~~1
05
IQ
ot
14
14
1.a
2.0
8.t
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