RESEARCH PAPER
Airborne spores of Basidiomycetes in Mérida (SW Spain)
 
More details
Hide details
1
Department of Plant Biology, Ecology and Earth Sciences, University of Extremadura, Badajoz, Spain
2
Environmental Biology and Public Health Department, University of Huelva, Huelva, Spain
3
Applied Physics Department, University of Extremadura, Badajoz, Spain
CORRESPONDING AUTHOR
Rafael Tormo Molina   

Department of Plant Biology, Ecology and Earth Sciences, University of Extremadura, Badajoz, Spain
 
Ann Agric Environ Med. 2013;20(4):657–663
KEYWORDS
ABSTRACT
The aim of this work was to detect the presence of Basidiomycetes spores (basidiospores, teliospores, uredospores and aeciospores) in Mérida (SW Spain) and assess the influence of weather parameters. Air was sampled continuously with a volumetric seven-day Burkard spore trap for two years. Fungi spores were identified and counted at x1,000 microscope resolution. Daily and weekly meteorological data and airborne spore concentration were analysed. Twenty-three spores types were identified, including basidiospores (Amanita, Agrocybe, Cortinarius, Coprinus -2 types-, Boletus, Bovista, Calvatia, Entoloma, Ganoderma, Inocybe, Russula, Scleroderma, Telephora), teliospores (Phragmidium, Tilletia, Ustillago -4 types-), uredospores, and aeciospores (2 types), all of these types of spores included different taxa. Average concentration was of 616 spores/m3, with maximum concentration in autumn (October), and a second concentration in spring (May-June); however, some spore types were more frequent in summer (Bovista, Ganoderma) or even in winter (Entoloma, Calvatia). The Amanita type was the most frequent (white-hyaline basidiospores); the second were teliospores of Ustilago, the third spore type was basidiospores of Coprinus (blackish basidiospores) and Agrocybe type (smoothed light to dark coloured basidiospores). Basidiospore concentration was positively correlated with temperature and negatively with relative humidity in most cases, and Ustilago teliospores concentration was positively correlated with wind speed. Differences in monthly rain were probably the origin between years. Airborne spores of Basidiomycetes may be separated into more than 20 types, and their seasonal concentration depended on meteorology as well as whether they were saprotrophic or parasitic.
 
REFERENCES (69)
1.
Kirk PM, Cannon PF, David JC, Stalpers J. Ainsworth and Bisby’s Dictionary of the Fungi. 9th ed. CAB International, Wallingford, UK., 2001.
 
2.
Gregory PH, Hirst JM. Possible role of basidiospores as airborne allergens. Nature. 1952; 170: 414.
 
3.
Herxheimer H, Frankfurt MD, Hyde HA, Cantab F, Williams, DA, Wales MSC. Allergic asthma caused by fungal spores. The Lancet. 1966; 287(7437): 572–573.
 
4.
Herxheimer H, Hyde HA, Williams DA. Allergic asthma caused by basidiospores. The Lancet. 1969; 294(7612): 131–133. doi:10.1016/S0140-6736(69)92441-6.
 
5.
Butcher BT, O’Neil CE, Reed MA, Altman LC, López M, Lehrer SB. Basidiomycete allergy: measurement of spore-specific IgE antibodies. J Allergy Clin Immunol. 1987; 80(6): 803–809.
 
6.
Giannini EH, Northey WT, Leather CR. The allergenic significance of certain fungi rarely reported as allergens. Ann Allergy. 1975; 35: 372.
 
7.
Horner WE, O‘neil CE, Lehrer SB. Basidiospore Aeroallergens. Clin Rev Allergy. 1992; 10: 191–211.
 
8.
Koivikko A, Savolainen J. Mushroom allergy. Allergy. 1988; 43(1): 1–10.
 
9.
Lehrer S, Horner E. Allergic reactions to basidiospores: identification of allergens. Aerobiologia. 1990; 6: 181–186.
 
10.
López M, Salvaggio J, Butchner BT. Allergenicity and immunogenicity of basidiomycetes. J Allergy Clin Immunol. 1976; 57(5): 480–488. doi:10.1016/0091-6749(76)90064-6.
 
11.
Saikai T, Tanaka H, Fuji M, Sugawara H, Takeya I, Tsunematsu K et al. Hypersensitivity pneumonitis induced by the spore of Pleurotus eryngii. Internat Med. 2002; 41(7): 571–573.
 
12.
Santilli J, Rockwell WJ, Collins RP. The significance of the spores of the basidiomycetes (mushrooms and their allies) in bronchial asthma and allergic rhinitis. Ann Allergy. 1985; 55: 469–471.
 
13.
Horner WE, Helbling A, Salvaggio JE, Lehrer SB. Fungal allergens. Clin Microbiol Rev. 1995; 8(2): 161–179.
 
14.
Osborne M, Reponen T, Adhikari A, Cho SH, Grinshpun SA, Levin L et al. Specific fungal exposures, allergic sensitization, and rhinitis in infants. Ped Allergy Immunol. 2006; 17(6): 450–457.
 
15.
Atkinson RW, Strachan DP, Anderson HR, Hajat S, Emberlin J. Temporal associations between daily counts of fungal spores and asthma exacerbations. Occupat Environm Med. 2006; 63(9): 580–590.
 
16.
Helbling A, Gayer F, Brander KA. Respiratory allergy to mushroom spores: not well recognized, but relevant. Ann Allergy Asthma Immunol. 1999; 83(1): 17–19.
 
17.
Newhouse CP, Levetin E. Correlation of environmental factors with asthma and rhinitis symptoms in Tulsa, OK. Ann Allergy Asthma Immunol. 2004; 92(3):356–66.
 
18.
Horner WE, Levetin E, Lehrer SB. Basidiospore allergen release: Elution from intact spores Original Research Article. J Allergy Clin Immunol. 1993; 92(2): 306–312.
 
19.
Crameri R, Weichel M, Flückiger S, Glaser AG, Rhyner C. Fungal allergies: a yet unsolved problem. Chem Immunol Allergy. 2006; 91: 121–133.
 
20.
Rivera-Mariani FE, Nazario-Jiménez S, López-Malpica F, Bolaños-Rosero B. Sensitization to airborne ascospores, basidiospores, and fungal fragments in allergic rhinitis and asthmatic subjects in San Juan, Puerto Rico. Int Arch Allergy Immunol. 2011; 155(4): 322–34.
 
21.
Helbling A, Gayer F, Pichler WJ, Brander KA. Mushroom (Basidiomycete) allergy: diagnosis established by skin test and nasal challenge. J Allergy Clin Immunol. 1998; 102(5): 853–858.
 
22.
Lehrer SB, López M, Butcher BT, Olson J, Reed M, Salvaggio JE. Basidiomycete mycelia and spore-allergen extracts: skin test reactivity in adults with symptoms of respiratory allergy. J Allergy Clin Immunol. 1986; 78(3): 478–485.
 
23.
Fischer B, Yawalkar N, Brander KA, Pichler WJ, Helbling A. Coprinus comatus (shaggy cap) is a potential source of aeroallergen that may provoke atopic dermatitis. J Allergy Clin Immunol. 1999; 104(4): 836–841.
 
24.
Davis WE, Horner WE, Salvaggio JE, Lehrer SB. Basidiospore allergens: analysis of Coprinus quadrifidus spore, cap, and stalk extracts. Clin Allergy. 1988; 18: 261–267.
 
25.
Lehrer SB, Hughes JM, Altman LC, Bousquet J, Davies RJ, Gell L et al. Prevalence of basidiomycete allergy in the USA and Europe and its relationship to allergic respiratory symptoms. Allergy. 1994; 49(6), 460–465.
 
26.
Gupta SK, Pereira BM, Singh AB. Fomes pectinatis: an aeroallergen in India. Asian Pacific Allergy Immunol. 1999; 17(1): 1–7.
 
27.
Hasnain SM, Newhook FJ, Wilson JD, Corbin JB. First report of Ganoderma allergenicity in New Zealand. New Zealand J Sci. 1984; 27: 261–267.
 
28.
Tarlo SM, Bell B, Srinizasan J, Dolovich J, Hargreave FE. Human sensitization to Ganoderma antigen. J Allergy Clin Immunol. 1979; 64: 43–49.
 
29.
Singh AB, Gupts SK, Pereira BMJ, Prakash D. Sensitization to Ganoderma lucidum in patients with respiratory allergy in India. Clin Exper Allergy. 1995; 25(5): 440–447.
 
30.
Mori S, Nakagawa-Yoshida K, Tsuchihashi H, Koreeda Y, Kawabata M, Nishiura Y et al. Mushroom worker’s lung resulting from indoor cultivation of Pleurotus osteatus. Occup Med (London). 1988; 48(7): 465–468.
 
31.
Yoshida K, Suga M, Yamasaki H, Nakamura K, Sato T, Kakishima M et al. Hypersensitivity pneumonitis induced by a smut fungus Ustilago esculenta. Thorax. 1996 51(6), 650–651.
 
32.
Ho TM, Tan BH, Ismail S, Bujang MK. Seasonal prevalence of air-borne pollen and spores in Kuala Lumpur, Malaysia. Asian Pacific J Allergy Immuno. 1995; 13(1): 17–22.
 
33.
McDevitt TJ, Mallea M, Dominick T, Holte KE. Allergic evaluation of cereal smuts. Ann Allergy. 1977; 38(1): 12–15.
 
34.
Sreeramulu T. Aerial dissemination of barley loose smut (Ustilago nuda). Trans British Mycol Soc. 1962; 45(3): 373–384.
 
35.
Smith RS. The liberation of cereal stem rust uredospores under various environmental conditions in a wind tunnel. Trans British Mycol Soc. 1966; 49(1): 33–41.
 
36.
Mills JT. Spore dispersal and natural infection in the oat loose smut (Ustilago avenae). Trans British Mycol Soc. 1967; 50(3): 403–412.
 
37.
Sreeramulu T, Vittal BPR. Spore dispersal of the sugarcane smut (Ustilago scitaminea). Trans British Mycol Soc. 1972; 58(2): 301–312.
 
38.
Mallaiah KV, Rao AS. Aerial dissemination of urediniospores of groundnut rust. Trans British Mycol Soc. 1982; 78(1): 21–28.
 
39.
Kramer CL, Pady SM, Clary R, Haard R. Diurnal periodicity in aeciospore release of certain rusts. Trans British Mycol Soc. 1968; 51(5): 679–687.
 
40.
Hirst JM. Aerobiology in plant pathology. Grana. 1991; 30(1): 25–29. doi: 10.1080/00173139109427765.
 
41.
Pady SM, Kramer CL. Kansas Aeromycology X: Basidiomycetes. Trans Kansas Acad Sci. 1960; 63(3): 125–134.
 
42.
Pady SM, Kramer CL. Sampling airborne fungi in Kansas for diurnal periodicity. Rev Palaeobot Palynol. 1967; 4: 227–232.
 
43.
Charpin H, Nolard N, Spieksma FThM, Stix E. Concentration urbaine des spores dans les pays de la Communauté Économique Européenne V. – Ustilago. Rev Française Allergol Immunol Clin. 1982; 22(1): 1–6.
 
44.
Levetin E. Studies on airborne basidiospores. Aerobiologia. 1990; 6(2): 177–180. doi: 10.1007/BF02539111.
 
45.
Levetin E. Identification and concentration of airborne basidiospores. Grana. 1991; 30(1): 123–128. doi: 10.1080/00173139109427785.
 
46.
Calderón MC, Lacey J, McCartney HA, Rosas I. Seasonal and diurnal variation of airborne basidiomycete spore concentrations in Mexico City. Grana. 1995; 34: 260–268.
 
47.
Crotzer V, Levetin E. The aerobiological significance of smut spores in Tulsa, Oklahoma. Aerobiologia. 1996; 12: 177–184.
 
48.
Craig F, Levetin E. Multi year study of Ganoderma aerobiology. Aerobiologia. 2000; 16: 75–81.
 
49.
Gonzalo MA, Paredes MM, Muñoz AF, Tormo R, Silva I. Dinámica de dispersión de basidiosporas en la atmósfera de Badajoz. Rev Española Alergol Inmunol Clín. 1997; 12(5): 294–300.
 
50.
Paredes MM, Martínez JF, Muñoz AF, Tormo R, Silva I. Presencia de esporas de Ustilago (Basidiomycetes) en Badajoz. Polen. 1998; 9: 35–42.
 
51.
Morales J, González FJ, Carrasco M, Ogalla VM, Candau P. Airborne basidiospores in the atmosphere of Seville (South Spain). Aerobiologia. 2006; 22(2): 127–134.
 
52.
Hasnain SM, Fatima K, Al-Frayh A, Al-Sedairy ST. Prevalence of airborne basidiospores in three coastal cities of Saudi Arabia. Aerobiologia. 2005; 21: 139–145.
 
53.
Stępalska D, Wołek J. Intradiurnal periodicity of fungal spore concentrations (Alternaria, Botrytis, Cladosporium, Didymella, Ganoderma) in Cracow, Poland. Aerobiologia. 2009; 25: 333–340.
 
54.
Hirst JM. An automatic volumetric spore trap. Ann Applied Biology. 1952; 39: 257–265.
 
55.
Tormo R, Muñoz AF, Silva I. Sampling in aerobiology. Differences between traverses along the lenght of the slide in Hirst sporetraps. Aerobiologia. 1996; 12: 161–166.
 
56.
Bassett IJ, Crompton CW, Parmelee JA. An Atlas of Airborne Pollen Grains and Common Fungus Spores of Canada. Canada Department of Agriculture, 1978.
 
57.
Grant-Smith E. Sampling and identifying allergenic pollens and moulds. San Antonio, TX: Blewstone Press, 1990.
 
58.
Parmasto E, Parmasto I; Mols T. Variation of Basidiospores in the Hymenomycetes and its significance to their taxonomy. Lubrecht & Cramer Ltd, 168 p., 1987.
 
59.
Pegler DN, Young TWK. Basidiospore morphology in the Agaricales. Lehre Cramer Ed., Nova Hedwigia. Beih, 263 p., 1971.
 
60.
Levetin E. Basidiospore identification. Ann Allergy. 1989; 62(4): 306–310.
 
61.
Quintero E, Rivera-Mariani F, Bolaños-Rosero B. Analysis of environmental factors and their effects on fungal spores in the atmosphere of a tropical urban area (San Juan, Puerto Rico). Aerobiologia. 2010; 26: 113–124.
 
62.
Gillum SJ, Levetin E. The air spora close to a compost facility in Northeast Oklahoma: Part I – spore trap sampling. Aerobiologia. 2008; 24: 3–12.
 
63.
Nayar TS, Mohan TK, Jothish PS. Status of airborne spores and pollen in a coir factory in Kerala, India. Aerobiologia. 2007; 23: 131–143.
 
64.
Oliveira MH, Ribeiro J, Delgado L, Abreu I. Seasonal and intradiurnal variation of allergenic fungal spores in urban and rural areas of the North of Portugal. Aerobiologia. 2009; 25: 85–98.
 
65.
Magyar D, Frenguelli G, Bricchi E, Tedeschini E, Csontos P, Li D-W, Bobvos J. The biodiversity of air spora in an Italian vineyard. Aerobiologia. 2009; 25: 99–109.
 
66.
Troutt C, Levetin E. Correlation of spring spore concentrations and meteorological conditions in Tulsa, Oklahoma. Int J Biometeorol. 2001; 45(2): 64–74.
 
67.
Li D-W. Release and dispersal of basidiospores from Amanita muscaria var. alba and their infiltration into a residence. Mycol Res. 2005; 109: 1235–1242.
 
68.
Grinn-Gofroń A, Mika A. Selected airborne allergenic fungal spores and meteorological factors in Szczecin, Poland, 2004–2006. Aerobiologia. 2008; 24: 89–97.
 
69.
Mordue JEM. Ustilospore ornamentation in the European genera of smut fungi. Trans British Mycol Soc. 1986; 87(3): 407–431.
 
eISSN:1898-2263
ISSN:1232-1966