Annals of West University of Timişoara, ser. Biology, 2016, vol. 19 (1), pp.87-100 87 METHODS OF BIOLOGICAL MONITORING IN URBAN CONDITIONS: QUANTIFICATION OF AIRBORNE FUNGAL SPORES Nicoleta IANOVICI Department of Biology - Chemistry; West University of Timisoara, Romania Corresponding author e-mail: [email protected]Received 5 April 2016; accepted 30 May 2016 ABSTRACT 85 fungi in outdoor air in the present study is reported. Over 44 taxa of anamorphic fungal spores were observed. The results of this study will contribute with information about existing mycoflora in atmosphere since knowing the local aeroallergens facilitates the diagnosis and treatment. KEY WORDS: airborne bioparticles, mycoflora INTRODUCTION Fungi and fungi-like organisms (Oomycetes and Plasmodiophoridae) can be beneficial as well as pathogenic. Fungi cause more plant diseases than any other group of plant pest with over 8,000 species shown to cause disease. However, a single plant species can be host to only a few fungal species, and similarly, most fungi usually have a limited host range (Knogge, 1999; Porta Puglia & Vannacci, 2012; Ianovici et al. 2010a; Ianovici et al. 2012). On the other hand, many fungi can attack insects and nematodes and may play an important role in keeping populations of these animals under control (Evans et al. 2011; Hughes et al. 2011). Some fungi are specialized parasites of microscopic animals in the soil (Barron, 1977). Fortunately, there are relatively few fungal pathogens of vertebrates (Voyles et al. 2009). Most fungi are associated with plants as saprotrophs and decomposers. An important group of fungi associated with plants is mycorrhizal fungi (Ianovici, 2010a). The rhizosphere is important not only for water and nutrient uptake but for interaction of the plant with soil biota, organic constituents, gases and minerals (Delvaux et al. 2005; Ianovici, 2010b; Ianovici et al. 2011). All plants in natural ecosystems probably have some type of symbiotic association with endophytic fungi (Rodriguez et al. 2009). In humans, there are several different types of fungal infections, or mycoses. Some fungi are members of the resident microflora in healthy people, but become pathogenic in people with predisposing conditions (Carris et al. 2012). The toxic effect of mycotoxins on human health is referred to as mycotoxicosis, the severity of which depends on the toxicity of the mycotoxin, the extent of exposure, age and nutritional status of the individual and possible synergistic effects of other chemicals to which the individual is exposed (Peraica et al. 1999; Filimon et al. 2012). The toxic effects of mycotoxins (e.g. ochratoxins, fumonisins, zearalenone, etc.) are mostly known from veterinary practice (Miscă et al. 2014). On the other hand, they are useful to man like a source of proteins, vitamins and amino acids, with high nutritional and functional value (Valverde et al, 2015). Most species make both meiospores (sexual) and mitospores (asexual) (Pringle, 2013). The asexually reproducing structures of a fungus are called anamorphs; sexual structures are known as teleomorphs (McGinnis & Tyring, 1996; Webster & Weber, 2007). The behaviour of
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Annals of West University of Timişoara, ser. Biology, 2016, vol. 19 (1), pp.87-100
87
METHODS OF BIOLOGICAL MONITORING IN URBAN
CONDITIONS: QUANTIFICATION OF AIRBORNE FUNGAL SPORES
Nicoleta IANOVICI
Department of Biology - Chemistry; West University of Timisoara, Romania
Corresponding author e-mail: [email protected] Received 5 April 2016; accepted 30 May 2016
ABSTRACT
85 fungi in outdoor air in the present study is reported. Over 44 taxa of anamorphic
fungal spores were observed. The results of this study will contribute with information
about existing mycoflora in atmosphere since knowing the local aeroallergens
facilitates the diagnosis and treatment.
KEY WORDS: airborne bioparticles, mycoflora
INTRODUCTION
Fungi and fungi-like organisms (Oomycetes and Plasmodiophoridae) can be beneficial
as well as pathogenic. Fungi cause more plant diseases than any other group of plant pest with
over 8,000 species shown to cause disease. However, a single plant species can be host to only
a few fungal species, and similarly, most fungi usually have a limited host range (Knogge,
1999; Porta Puglia & Vannacci, 2012; Ianovici et al. 2010a; Ianovici et al. 2012). On the other hand, many fungi can attack insects and nematodes and may play an important role in keeping
populations of these animals under control (Evans et al. 2011; Hughes et al. 2011). Some fungi
are specialized parasites of microscopic animals in the soil (Barron, 1977). Fortunately, there
are relatively few fungal pathogens of vertebrates (Voyles et al. 2009). Most fungi are
associated with plants as saprotrophs and decomposers. An important group of fungi associated
with plants is mycorrhizal fungi (Ianovici, 2010a). The rhizosphere is important not only for water and nutrient uptake but for interaction of the plant with soil biota, organic constituents,
gases and minerals (Delvaux et al. 2005; Ianovici, 2010b; Ianovici et al. 2011). All plants in
natural ecosystems probably have some type of symbiotic association with endophytic fungi
(Rodriguez et al. 2009). In humans, there are several different types of fungal infections, or
mycoses. Some fungi are members of the resident microflora in healthy people, but become
pathogenic in people with predisposing conditions (Carris et al. 2012). The toxic effect of mycotoxins on human health is referred to as mycotoxicosis, the severity of which depends on
the toxicity of the mycotoxin, the extent of exposure, age and nutritional status of the individual
and possible synergistic effects of other chemicals to which the individual is exposed (Peraica
et al. 1999; Filimon et al. 2012). The toxic effects of mycotoxins (e.g. ochratoxins, fumonisins,
zearalenone, etc.) are mostly known from veterinary practice (Miscă et al. 2014). On the other
hand, they are useful to man like a source of proteins, vitamins and amino acids, with high nutritional and functional value (Valverde et al, 2015).
Most species make both meiospores (sexual) and mitospores (asexual) (Pringle, 2013).
The asexually reproducing structures of a fungus are called anamorphs; sexual structures are
known as teleomorphs (McGinnis & Tyring, 1996; Webster & Weber, 2007). The behaviour of
IANOVICI: Methods of biological monitoring in urban conditions: quantification of airborne fungal spores
88
any particle in the atmosphere depend upon its size, density and shape. Most fungi are well
adapted for wind spore dissemination (Cecchi et al. 2010).
Generally, air sampling may be conducted for qualitative or quantitative purposes. The aim of qualitative sampling is to determine the presence of no specific airborne fungi, while
quantitative sampling aims at measuring the concentration of selected types of spores. Analyses
of aeroallergens in Romania have been made since 1999 but only a few studies have been
carried out on airborne fungi. Ianovici & Faur (2003) used a volumetric method for the first
time in a Romanian study during their investigation of atmospheric fungal spores in the city of
Timisoara. Subsequently, one study took into account the comparison of spore concentrations in cities Brasov, Bucharest, Craiova and Timisoara for summer 2005 (Ianovici et al. 2011). A
second study compared the concentrations of airborne spores and pollen in the cities of Brasov,
Bucharest, Cluj-Napoca and Timisoara in 2008 (Ianovici et al. 2013). More recently it outlined
the dynamics of fungal spore concentrations in relation to meteorological factors for the period
between 2008-2010 (Ianovici, 2016). In Timisoara have been many investigations to determine
the presence of allergenic species of fungi and to evaluate their seasonal variations (Faur et al. 2003; Ianovici et al. 2004; Ianovici et al. 2007; Ianovici & Dumbravă, 2008a; Ianovici &
response relationships between exposure to airborne spores and symptoms are lacking (Codina
et al. 2008). The knowledge on diurnal, seasonal and annual fluctuations in airborne spores in
any geographical area is essential for effective diagnosis and treatment of allergy.
Over time we tested a number of methods useful in biomonitoring urban habitat quality: dynamics of airborne bioparticles concentrations (Ianovici et al. 2015a), quantification
of colonization with vesicular arbuscular mycorrhizae (Ianovici, 2010), estimation of pollen
viability, determination of several anatomical and physiological traits of plants (density of
stomata, density of trichomes, relative water content, ash content, relative saturation deficit,
succulence, water loss, specific leaf area, specific leaf weight, leaf thickness, leaf thickness lost, leaf area, fractal dimension, tissue density) (Ianovici et al. 2015b). The objective of this study
was to identify the fungal spores found in Timisoara atmosphere.
MATERIALS AND METHODS
Timisoara's urban vegetation is mainly represented by ornamental park vegetation,
gardens close to houses and vegetation along foothpaths and roads. Identification of airborne spores was performed using a 7-day volumetric trap (VPPS-2000, Lanzoni) set on the roof of
the West University in Timisoara, approximately 20 m above ground level. The qualitative
compositions of the samples were determined under a light microscope with ×400
magnification (Ianovici, 2015c).
RESULTS AND DISCUSSIONS
In the recent years, air quality has become an important environmental health issue
which in part is related to numerous human diseases (Ianovici & Faur, 2001; Chadeganipour et
al. 2010). The aeroallergens are predominantly constituted by pollen grains of plants and fungal
spores (Ong et al, 1995; Ianovici, 2007). In the last years, attention to air pollution, not just by
chemical and physical pollutants but also by fungal spores and pollen grains, has increased. Airborne fungal spores are considered as indicators of the level of atmospheric bio-pollution
Annals of West University of Timişoara, ser. Biology, 2016, vol. 19 (1), pp.87-100
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(Ianovici & Tudorica, 2009; Grinn-Gofroń & Strzelczak, 2011). It is known that most of the
allergenic fungi are classified under Ascomycetes and Deuteromycetes with a few in
Basidiomycetes (Kurup et al. 2000). Repeated exposures to large concentrations of spores may cause severe symptoms of respiratory allergy.
The airborne fungal genera are listed in Table 1.
TABLE 1.The fungal spore types that were identified in air samples
FIG 4. Airborne fungi detected in outdoor environment
Anamorphs: B Bipolaris Shoemaker 1959; Teleomorphs: A Melanomma Nitschke ex Fuckel 1870, C Caloplaca Th. Fr. 1860, D Chaetosphaerella E. Müll. & C. Booth 1972
Annals of West University of Timişoara, ser. Biology, 2016, vol. 19 (1), pp.87-100
93
FIG 5. Airborne fungi detected in outdoor environment
Anamorphs: F Curvularia Boedijn 1933, H Dendryphiella Bubák & Ranoj. 1914, J Diplodia Fr. 1834, K Exserohilum K.J. Leonard & Suggs 1974; Teleomorphs: E Paraphaeosphaeria Erikss. 1967, G Delitschia Auersw. 1866, I
Diatrype Fr. 1849, L Farlowiella Sacc. 1891,
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94
FIG 6. Airborne fungi detected in outdoor environment
Anamorphs: M Helicoma Corda 1837, P Periconia Tode 1791, R Pestalotiopsis Steyaert 1949, S Prosthemium Kunze 1817; Teleomorphs: N Heptameria Rehm & Thüm. 1879, O Massaria De Not. 1844, T Rosellinia De Not. 1844
(Xylariaceae), U Rutstroemia P. Karst. 1871,
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FIG 7. Airborne fungi detected in outdoor environment
Anamorphs: V Pseudocercospora Speg. 1910, X Sporidesmium Link 1809, W Asterosporium Kunze 1819; Teleomorphs: Z Sporormiella Ellis & Everh. 1892,
A few papers reported on the impact of airborne fungi on monuments and rock
surfaces in indoor and outdoor environments (Mandrioli & Zenotti Censoni, 1982; Urzi et al.
2001). Among biological agents, fungi are responsible for the destruction of cultural heritage objects located in outdoor environments. They can cause damage on the stone surface such as
formation of biofilms, chemical reactions with the substrate, physical penetration into the
substrate as well as pigment production (Pandey et al, 2011). RIF (rock-inhabiting fungi) are
active biological agents causing visible alteration patterns and exfoliation of stone monuments
(Onofri et al, 2014). Other researches showed that airborne fungal sporres are implicated in the
damage of food commodities and stored products (Pyrri & Kapsanaki-Gotsi, 2007; Atanda et
al, 2011). Fungi may cause heavy loss to bakery products and raw materials (Jain, 2000;
Cornea et al, 2011). Since the most common factor of bakery products is water activity,
microbiological spoilage, in particular fungi growth is the major economical importance of
bakery products (Saranraj & Geetha, 2012). A large number of airborne fungi have been found
to be responsible for the deterioration of organic material in indoor environments. Deterioration
of library materials has caused great concern to workers at different places (Gutcho, 1974). For example, an article identifies moulds as the most important biodeteriorating agents of library
materials (Bankole, 2010). In addition to destroying, disfiguring and staining books, the fungi
have been linked to numerous adverse human health effects that fall into three categories:
allergic, toxic and infectious. Bio-deterioration of library materials is a worldwide problem and
IANOVICI: Methods of biological monitoring in urban conditions: quantification of airborne fungal spores
96
it is a great damage especially to unique manuscripts and books stored in the libraries
(Shamsian et al, 2006; Ebrahimi et al, 2012).
Airborne bioparticles are major vectors for human, animal, and plant diseases but they have been detected in clouds, fog, rain and snowfall. Recent atmospheric researches show that
the ice-nucleating activity may emanate from suspendable macromolecules that can be
extracted from the airborne bioparticles (pollen grains, fungal spores, bacteria, plant debris etc.)
(Hader et al. 2014). If biological ice nuclei are abundant in the atmosphere they can influence
the hydrological cycle and may play an important role in regionally precipitation (Huffman et
al. 2013). Several investigations have highlighted the potential implication of airborne bioparticles in ice cloud formation and the need to quantify the number and source of biological
ice nuclei in the air (Iannone et al. 2011).
Airborne fungal spores originate from soil, plants, and vegetal and animal remains.
Many works report that dead grasses, dead wood, animal and bird dead, leaves, fruits, tree bark,
soil particles, feces and debris, provide adequate substrate for a wide variety of fungi in outdoor
sites. Airborne spore concentrations are determined by the proximity of substrate, growth and development of colonies and fruiting structures, method of spore release, dispersal, and
deposition and how these are affected by the effect of vertical temperature gradient of the air
(Khattab & Levetin 2008). Changes in fungal phenology vary between regions (Boddy et al.
2014). Different parts of habitat may differ in their microclimate, susceptibility to microbial
colonization and nutrient availability, pH, light, disturbance, therefore changes in the
environment cause differences in diversity. It is not certain that all variation in spore concentrations can be explained by meteorological variables only. The increase in fungal spore
concentrations also may be related to the maturing of tree foliage, grasses and local crops.
Spore concentrations may depend on the state of the host and the weatherings on the host
plants. Further, more extensive studies are necessary in order to evaluate the effects of floristic
patterns on the fungal flora (Das & Gupta-Bhattacharya, 2012). Many spores trapped are likely to come from sources outside the city and are carried by wind to the city centre. The harvest
season, grain storage and handling are agricultural practices that may introduce very large
concentrations of specific spore types into the air. The rupture of fungal spores, or rising air
currents, may return aeroallergens from the ground into the air (Marks et al. 2001). Outdoor
airborne fungi sometimes influence the levels of airborne concentration in indoors (Al-Qurashi
2007). Some authors report that types and concentrations of fungi that affect indoor air quality are similar to those found in outdoor air and fungi may occur in homes without dampness
problems (Ayanbimpe et al. 2010).
Atmospheric fungal spores constitute an important component of airborne bioparticles,
occur widely and in greater concentration than pollens (Ianovici et al. 2013a). In general, pollen
and spore concentrations are expected to gradually rise in response to higher levels of CO2
(Klironomos et al. 1997; Ianovici, 2007). There may be a number of indirect effects on fungal growth, reproduction, spore production and dissemination as a result of plant changes under
increased atmospheric CO2 concentration as well as feedback and interactions among plants,
fungi, and abiotic factors (Stiling & Cornelissen 2007; Cecchi et al. 2010). It is expected that an
increase in global temperatures and changes in rainfall distribution may lead to significant
changes in fungal species distribution patterns (Boddy et al. 2014). Climate change may facilitate the emergence of fungal plant pathogens through the dispersal of pathogens to new
Annals of West University of Timişoara, ser. Biology, 2016, vol. 19 (1), pp.87-100
97
locations and/or through habitat modifications for both pathogens and plants. There may be
mentioned changes in habitat / substrate preferences, changes in yields of fruit bodies or
changes in fungal phenology. Some studies from Norway and the UK have reported shifts in the phenology of fungus fruiting bodies over the last 50 years (Kauserud et al. 2010).
Numerous fungi animal pathogens have gone through dramatic changes and for some species it
has been speculated that climate change may have a role (Pounds et al. 2006). On the other
hand, there is increasing evidence that climate change will be a key issue in how fungal plant
pathogens will affect food security and ecosystem health.
CONCLUSIONS
The present study has an important contribution for determination of levels and types
of airborne fungi in Timişoara (Romania).
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