methods of biological monitoring in urban conditions: quantification

Annals of West University of Timişoara, ser. Biology, 2016, vol. 19 (1), pp.87-100

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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

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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 &

Dumbravă, 2008b; Ianovici, 2008; Ianovici et al. 2008; Ianovici & Tudorica, 2009). Dose-

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


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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

Anamorphs fungi Teleomorphs fungi

1. Alternaria Nees 1817 2. Aspergillus Micheli ex Haller 1768 3. Asperisporium Maubl. 1913 4. Asterosporium Kunze 1819 5. Bipolaris Shoemaker 1959 6. Bispora Corda 1837 7. Botrytis Micheli ex Haller 1768 8. Ceratosporium Schwein. 1832 9. Cercospora Fresen. 1863 10. Cercosporella Sacc. 1880 11. Chaetoconis Clem. 1909 12. Cladosporium Link 1816 13. Corynespora Güssow 1906 14. Curvularia Boedijn 1933 15. Dendryphiella Bubák & Ranoj. 1914 16. Diplodia Fr. 1834 17. Drechslera S. Ito 1930 18. Epicoccum Link 1815 19. Exosporium Link 1809 20. Exserohilum Leonard & Suggs 1974 21. Fusariella Sacc. 1884 22. Fusarium Link 1809 23. Fusichalara Hughes & Nag Raj 1973 24. Fusicladium Bonord. 1851 25. Helicoma Corda 1837 26. Helicomyces Link, 1809 27. Helminthosporium Link 1809 28. Microsporum Gruby 1843 29. Monodictys Hughes 1958 30. Nigrospora Zimm. 1902 31. Oidium Link 1809 32. Penicillium Link 1809 33. Periconia Tode 1791 34. Pestalotiopsis Steyaert 1949 35. Piricauda Bubák 1914 36. Pithomyces Berk. & Broome 1875 37. Polythrincium Kunze 1817 38. Prosthemium Kunze 1817 39. Pseudocercospora Speg. 1910 40. Sporidesmium Link 1809 41. Stachybotrys Corda 1837 42. Stemphylium Wallr. 1833 43. Torula Pers. 1794 44. Ulocladium Preuss 1851

Ascospores 1. Amphisphaeria Ces. & De Not. 1863 2. Arenariomyces Höhnk 1954 3. Ascobolus Pers. 1796 4. Caloplaca Th. Fr. 1860 5. Capronia Sacc. 1883 6. Chaetomium Kunze 1817 7. Chaetosphaerella Müll. & Booth 1972 8. Comoclathris Clem. 1909 9. Delitschia Auersw. 1866 10. Diatrype Fr. 1849 11. Didymella Sacc., 1880 12. Didymosphaeria Fuckel, 1870 13. Farlowiella Sacc. 1891 14. Heptameria Rehm & Thüm. 1879 15. Gloniella Sacc. 1883 16. Glonium Muhl., 1813 17. Hysterium Tode, 1791 18. Hysterographium Corda, 1842 19. Leptosphaeria Ces. & De Not. 1863 20. Lophiostoma Ces. & De Not. 1863 21. Massaria De Not. 1844 22. Massarina Sacc. 1883 23. Massariosphaeria (Müll.) Crivelli 1983 24. Melanomma Nitschke ex Fuckel 1870 25. Melogramma Fr. 1849 26. Mytilidion Sacc. 1875 27. Paraphaeosphaeria Erikss. 1967 28. Phaeosphaeria Miyake 1909 29. Pleospora Rabenh. ex Ces. & De Not. 30. Podosordaria Ellis & Golw., 1897 31. Rosellinia De Not. 1844 32. Rutstroemia Karst. 1871 33. Sporormiella Ellis & Everh. 1892 34. Trichodelitschia Munk 1953 35. Venturia Sacc. 1882

Basidiospores 1. Agrocybe Fayod 1889 2. Ganoderma Karst. 1881 3. Puccinia Pers. 1801 4. Tilletia Tul. & Tul. 1847 5. Uromyces (Link) Unger 1833


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FIG.1. Airborne fungi detected in Timisoara (Ianovici & Tudorica, 2009)

(A- Alternaria type; B- Drechslera/Helminthosporium type; C- Cladosporium type; D- Nigrospora type; E- Torula

type; F- Peronospora type;


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G- Pithomyces type; H- Stemphylium type; I- Bispora type; J- Capronia type; K- Neohendersonia type; L- Amphisphaeria type


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M- Fusarium/Leptosphaeria type; N- Epicoccum type)

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


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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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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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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


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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


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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