pp 1–17 | Cite as

Airborne Cladosporium and Alternaria spore concentrations through 26 years in Copenhagen, Denmark

  • Yulia OlsenEmail author
  • Carsten Ambelas Skjøth
  • Ole Hertel
  • Karen Rasmussen
  • Torben Sigsgaard
  • Ulrich Gosewinkel
Original Paper


Cladosporium spp. and Alternaria spp. spores are dominating the airspora of Denmark. Currently, little is known about the influence of climate change on the fungal spore abundance in the air. The aim of this study was to examine temporal changes in airborne Alternaria and Cladosporium spores over 26 years. This is the first report of long-term airborne Cladosporium spore occurrence in Denmark. Air spore concentrations were obtained with a Burkard volumetric spore sampler placed in Copenhagen, Denmark, during June–September, 1990–2015. The highest monthly Spore integrals (SIn) for Alternaria were measured in August, whereas for Cladosporium July SIn was nearly as high as August SIn. Average Alternaria seasonal spore integral (SSIn) was 8615 Spores day m−3, while average 3-month (July–September) Cladosporium SIn was 375,533 Spores day m−3. Despite increasing annual temperature and decreasing relative humidity, we found a decreasing trend for Alternaria seasonal SIn (Slope = − 277, R2 = 0.38, p < 0.05), Alternaria (Slope = − 31, R2 = 0.27, p < 0.05) and Cladosporium (Slope = − 440, R2 = 0.23, p < 0.05) annual peak concentrations. We did not find any statistically significant trends for airborne Alternaria seasonal characteristics and duration, and likewise for Cladosporium 3-month SIn and peak concentration dates. Mean temperature was the main meteorological factor affecting daily spore concentrations. However, effect of meteorological parameters on daily spore concentrations was stronger for Cladosporium (R2 = 0.41) than for Alternaria (R2 = 0.21). Both genera had diurnal peaks during the day hours, earlier for Cladosporium (11:30–14:30) and later for Alternaria (15:00–19:00). Although Alternaria and Cladosporium daily concentrations were moderately correlated (Spearman’s correlation coefficient: rs = 0.55, p < 0.05), their overall annual indices were different, which indicates different sources and different factors determining spore release. We explain temporal decreasing trends in Alternaria SSIn by growing urbanisation around Copenhagen and by changes in agricultural practices.


Cladosporium Alternaria Annual trends Climate change Respiratory allergy Land use 



We thank K. Mortensen, R. Keller and C. Nordstrøm for providing the meteorological data from the HCØ station.

Supplementary material

10453_2019_9618_MOESM1_ESM.docx (120 kb)
Supplementary file1 (DOCX 120 kb)


  1. Aira, M.-J., Rodríguez-Rajo, F.-J., Fernández-González, M., Seijo, C., Elvira-Rendueles, B., Gutiérrez-Bustillo, M., et al. (2012). Cladosporium airborne spore incidence in the environmental quality of the Iberian Peninsula. Grana,51(4), 293–304.CrossRefGoogle Scholar
  2. Aira, M.-J., Rodríguez-Rajo, F.-J., Fernández-González, M., Seijo, C., Elvira-Rendueles, B., Abreu, I., et al. (2013). Spatial and temporal distribution of Alternaria spores in the Iberian Peninsula atmosphere, and meteorological relationships: 1993–2009. International Journal of Biometeorology,57(2), 265–274.CrossRefGoogle Scholar
  3. Almeida, E., Caeiro, E., Todo-Bom, A., Ferro, R., Dionísio, A., Duarte, A., et al. (2018). The influence of meteorological parameters on Alternaria and Cladosporium fungal spore concentrations in Beja (Southern Portugal): Preliminary results. Aerobiologia,34(2), 219–226.CrossRefGoogle Scholar
  4. Atkinson, R. W., Strachan, D. P., Anderson, H. R., Hajat, S., & Emberlin, J. (2006). Temporal associations between daily counts of fungal spores and asthma exacerbations. Occupational and Environmental Medicine,63(9), 580–590.CrossRefGoogle Scholar
  5. Awad, A. H. A. (2005). Vegetation: A source of air fungal bio-contaminant. Aerobiologia,21(1), 53–61.CrossRefGoogle Scholar
  6. Bagni, N., Davies, R., Mallea, M., Nolard, N., Spireksma, F., & Stix, E. (1977). Spore concentration in cities of the European Economic Community. II. Spores of Cladosporium and Alternaria. Acta Allergologica, 32(2), 118–138.CrossRefGoogle Scholar
  7. Bardei, F., Bouziane, H., Trigo, M. D. M., Ajouray, N., El Haskouri, F., & Kadiri, M. (2017). Atmospheric concentrations and intradiurnal pattern of Alternaria and Cladosporium conidia in Tétouan (NW of Morocco). Aerobiologia,33(2), 221–228.CrossRefGoogle Scholar
  8. Bednarz, A., & Pawlowska, S. (2016). A fungal spore calendar for the atmosphere of Szczecin, Poland. Acta Agrobotanica,69(3), 1–9.CrossRefGoogle Scholar
  9. Boddy, L., Büntgen, U., Egli, S., Gange, A. C., Heegaard, E., Kirk, P. M., et al. (2014). Climate variation effects on fungal fruiting. Fungal Ecology,10, 20–33.CrossRefGoogle Scholar
  10. Bruffaerts, N., De Smedt, T., Delcloo, A., Simons, K., Hoebeke, L., Verstraeten, C., et al. (2018). Comparative long-term trend analysis of daily weather conditions with daily pollen concentrations in Brussels, Belgium. International Journal of Biometeorology,62(3), 483–491.CrossRefGoogle Scholar
  11. Busck, A. G., Kristensen, S. P., Præstholm, S., Reenberg, A., & Primdahl, J. (2006). Land system changes in the context of urbanisation: Examples from the peri-urban area of Greater Copenhagen. Geografisk Tidsskrift-Danish Journal of Geography,106(2), 21–34.CrossRefGoogle Scholar
  12. Cappelen, J., Kern-Hansen, C., Laursen, E. V., Jørgensen, P. V., Jørgensen, P. V., & Jørgensen, B. V. (2017). DMI report 17-02. In C. John (Ed.), Denmark—DMI Historical Climate Data Collection 1768–2016. Copenhagen, Denmark: Danish Meteorological Institute.Google Scholar
  13. Cecchi, L., D’Amato, G., Ayres, J., Galan, C., Forastiere, F., Forsberg, B., et al. (2010). Projections of the effects of climate change on allergic asthma: The contribution of aerobiology. Allergy,65(9), 1073–1081.Google Scholar
  14. Chrenová, J., Mišík, M., Ščevková, J., Mičieta, K., & Mlynarčík, D. (2004). Monitoring of microscopic airborne fungi in Bratislava. Acta Facultatis Pharmaceuticae Universitatis Comenianae,51, 68–72.Google Scholar
  15. Corden, J. M., & Millington, W. M. (2001). The long-term trends and seasonal variation of the aeroallergen Alternaria in Derby, UK. Aerobiologia,17(2), 127–136.CrossRefGoogle Scholar
  16. Corden, J. M., Millington, W. M., & Mullins, J. (2003). Long-term trends and regional variation in the aeroallergen Alternaria in Cardiff and Derby UK—Are differences in climate and cereal production having an effect? Aerobiologia,19(3/4), 191–199.CrossRefGoogle Scholar
  17. Crameri, R., Garbani, M., Rhyner, C., & Huitema, C. (2014). Fungi: The neglected allergenic sources. Allergy,69(2), 176–185.CrossRefGoogle Scholar
  18. D’Amato, G., Holgate, S. T., Pawankar, R., Ledford, D. K., Cecchi, L., Al-Ahmad, M., et al. (2015). Meteorological conditions, climate change, new emerging factors, and asthma and related allergic disorders. A statement of the World Allergy Organization. World Allergy Organization Journal,8(1), 1.Google Scholar
  19. D’Amato, M., Cecchi, L., Annesi-Maesani, I., & D’Amato, G. (2018). News on climate change, air pollution, and allergic triggers of asthma. Journal of Investigational Allergology and Clinical Immunology,28(2), 91–97.CrossRefGoogle Scholar
  20. Damialis, A., Mohammad, A. B., Halley, J. M., & Gange, A. C. (2015a). Fungi in a changing world: Growth rates will be elevated, but spore production may decrease in future climates. International Journal of Biometeorology,59(9), 1157–1167.CrossRefGoogle Scholar
  21. Damialis, A., Vokou, D., Gioulekas, D., & Halley, J. M. (2015b). Long-term trends in airborne fungal-spore concentrations: A comparison with pollen. Fungal Ecology,13, 150–156.CrossRefGoogle Scholar
  22. Ellermann, T., Nygaard, J., Nøjgaard, J. K., Nordstrøm, C., Brandt, J., Christensen, J., et al. (2016). The Danish Air Quality Monitoring Programme. Annual Summary for 2015. Scientific Report from DCE—Danish Centre for Environment and Energy No. 201 (pp. 65). Aarhus University, DCE—Danish Centre for Environment and Energy.Google Scholar
  23. Fernández-Rodríguez, S., Sadyś, M., Smith, M., Tormo-Molina, R., Skjøth, C. A., Maya-Manzano, J. M., et al. (2015). Potential sources of airborne Alternaria spp. spores in South-west Spain. Science of The Total Environment,533, 165–176.CrossRefGoogle Scholar
  24. Fertner, C. (2012). Urbanisation, urban growth and planning in the Copenhagen Metropolitan Region with reference studies from Europe and the USA. Forest & Landscape, University of Copenhagen. Forest and landscape research, No. 54/2012.Google Scholar
  25. Fleming, Z. L., Monks, P. S., & Manning, A. J. (2012). Review: Untangling the influence of air-mass history in interpreting observed atmospheric composition. Atmospheric Research, 104–105, 1–39.CrossRefGoogle Scholar
  26. Friesen, T. L., De Wolf, E. D., & Francl, L. J. (2001). Source strength of wheat pathogens during combine harvest. Aerobiologia,17(4), 293–299.CrossRefGoogle Scholar
  27. Galan, C., Ariatti, A., Bonini, M., Clot, B., Crouzy, B., Dahl, A., et al. (2017). Recommended terminology for aerobiological studies. Aerbiologia,33, 293–295.CrossRefGoogle Scholar
  28. García-Mozo, H., Yaezel, L., Oteros, J., & Galán, C. (2014). Statistical approach to the analysis of olive long-term pollen season trends in southern Spain. Science of The Total Environment,473, 103–109.CrossRefGoogle Scholar
  29. Giner, M. M., García, J. C., & Camacho, C. N. (2001). Airborne Alternaria spores in SE Spain (1993–98). Occurrence patterns, relationship with weather variables and prediction models. Grana,40(3), 111–118.CrossRefGoogle Scholar
  30. Gravesen, S. (1979). Fungi as a cause of allergic disease. Allergy,34(3), 135–154.CrossRefGoogle Scholar
  31. Grinn-Gofroń, A., & Mika, A. (2008). Selected airborne allergenic fungal spores and meteorological factors in Szczecin, Poland, 2004–2006. Aerobiologia,24(2), 89.CrossRefGoogle Scholar
  32. Grinn-Gofroń, A., Nowosad, J., Bosiacka, B., Camacho, I., Pashley, C., Belmonte, J., et al. (2019). Airborne Alternaria and Cladosporium fungal spores in Europe: Forecasting possibilities and relationships with meteorological parameters. Science of The Total Environment,653, 938–946.CrossRefGoogle Scholar
  33. Heinzerling, L. M., Burbach, G. J., Edenharter, G., Bachert, C., Bindslev-Jensen, C., Bonini, S., et al. (2009). GA2LEN skin test study I: GA2LEN harmonization of skin prick testing: novel sensitization patterns for inhalant allergens in Europe. Allergy,64(10), 1498–1506.CrossRefGoogle Scholar
  34. Hirst, J. M. (1952). An automatic volumetric spore trap. Annals of Applied Biology,39(2), 257–265.CrossRefGoogle Scholar
  35. Hollins, P., Kettlewell, P., Atkinson, M., Stephenson, D., Corden, J., Millington, W., et al. (2004). Relationships between airborne fungal spore concentration of Cladosporium and the summer climate at two sites in Britain. International Journal of Biometeorology,48(3), 137–141.CrossRefGoogle Scholar
  36. Kasprzyk, I. (2008). Aeromycology—Main research fields of interest during the last 25 years. Annals of Agricultural and Environmental Medicine,15(1), 1–7.Google Scholar
  37. Kasprzyk, I., & Worek, M. (2006). Airborne fungal spores in urban and rural environments in Poland. Aerobiologia,22, 169–176.CrossRefGoogle Scholar
  38. Kasprzyk, I., Sulborska, A., Nowak, M., Szymanska, A., Kaczmarek, J., Haratym, W., et al. (2013). Fluctuation range of the concentration of airborne Alternaria condiospores sampled at different geographical locations in Poland (2010–2011). Acta Agrobotanica,66(1), 65–76.CrossRefGoogle Scholar
  39. Kasprzyk, I., Kaszewski, B. M., Weryszko-Chmielewska, E., Nowak, M., Sulborska, A., Kaczmarek, J., et al. (2016). Warm and dry weather accelerates and elongates Cladosporium spore seasons in Poland. Aerobiologia,32(1), 109–126.CrossRefGoogle Scholar
  40. Katotomichelakis, M., Nikolaidis, C., Makris, M., Proimos, E., Aggelides, X., Constantinidis, T. C., et al. (2016). Alternaria and Cladosporium calendar of Western Thrace: Relationship with allergic rhinitis symptoms. The Laryngoscope,126(2), E51–E56.CrossRefGoogle Scholar
  41. Larsen, L., & Gravesen, S. (1991). Seasonal variation of outdoor airborne viable microfungi in Copenhagen, Denmark. Grana,30(2), 467–471.CrossRefGoogle Scholar
  42. Levetin, E., Horner, W. E., Scott, J. A., Barnes, C., Baxi, S., Chew, G. L., et al. (2016). Taxonomy of Allergenic Fungi. The Journal of Allergy and Clinical Immunology: In Practice, 4(3), 375–385.e371.Google Scholar
  43. Mitakakis, T. Z., Clift, A., & McGee, P. A. (2001). The effect of local cropping activities and weather on the airborne concentration of allergenic Alternaria spores in rural Australia. Grana,40(4–5), 230–239.CrossRefGoogle Scholar
  44. Nilsson, S., & Persson, S. (1981). Tree pollen spectra in the Stockholm region (Sweden), 1973–1980. Grana,20(3), 179–182.CrossRefGoogle Scholar
  45. O'Connor, D. J., Sadyś, M., Skjøth, C., Healy, D. A., Kennedy, R., & Sodeau, J. R. (2014). Atmospheric concentrations of Alternaria, Cladosporium, Ganoderma and Didymella spores monitored in Cork (Ireland) and Worcester (England) during the summer of 2010. Aerobiologia,30(4), 397–411.CrossRefGoogle Scholar
  46. Olesen, M., Madsen, K. C., Ludwigsen, C. A., Boberg, F., Christensen, T., Cappelen, J., et al. (2014). Fremtidige klimaforandringer i Danmark. Damarks Klimacenter rapport nr. 6 Copenhagen: Danmarks Meteorologiske Institut.Google Scholar
  47. Oliveira, M., Ribeiro, H., Delgado, J. L., & Abreu, I. (2009). Seasonal and intradiurnal variation of allergenic fungal spores in urban and rural areas of the North of Portugal. Aerobiologia,25(2), 85–98.CrossRefGoogle Scholar
  48. Olsen, Y., Begovic, T., Skjøth, C. A., Rasmussen, K., Gosewinkel, U., Hertel, O., et al. (2019a). Grain harvesting as a local source of Cladosporium spp. in Denmark. Aerobiologia,35(2), 373–378.CrossRefGoogle Scholar
  49. Olsen, Y., Gosewinkel, U., Skjøth, C. A., Hertel, O., Rasmissen, K., & Sigsgaard, T. (2019b). Regional variation in airborne Alternaria spore concentrations in Denmark through 2012–2015 seasons: the influence of meteorology and grain harvesting. Aerobiologia,35(3), 533–551.CrossRefGoogle Scholar
  50. Peternel, R., Culig, J., & Hrga, I. (2003). Atmospheric concentrations of Cladosporium spp. and Alternaria spp. spores in Zagreb (Croatia) and effects of some meteorological factors. Annals of agricultural and environmental medicine AAEM,11(2), 303–307.Google Scholar
  51. Rasmussen, A. (2002). The effects of climate change on the birch pollen season in Denmark. Aerobiologia,18(3), 253–265.CrossRefGoogle Scholar
  52. Reyes, E. S., de la Cruz, D. R., Merino, E., & Sánchez, J. S. (2009). Meteorological and agricultural effects on airborne Alternaria and Cladosporium spores and clinical aspects in Valladolid [Spain]. Annals of Agricultural and Environmental Medicine,16(1), 53–61.Google Scholar
  53. Rizzi-Longo, L., Pizzulin-Sauli, M., & Ganis, P. (2009). Seasonal occurrence of Alternaria [1993-2004] and Epicoccum [1994–2004] spores in Trieste [NE Italy]. Annals of Agricultural and Environmental Medicine,16(1), 63–70.Google Scholar
  54. Rodríguez-Rajo, F. J., Iglesias, I., & Jato, V. (2005). Variation assessment of airborne Alternaria and Cladosporium spores at different bioclimatical conditions. Mycological Research,109(4), 497–507.CrossRefGoogle Scholar
  55. Sadyś, M. (2017). Effects of wind speed and direction on monthly fluctuations of Cladosporium conidia concentration in the air. Aerobiologia,33(3), 445–456. Scholar
  56. Sadyś, M., Skjøth, C. A., & Kennedy, R. (2015). Determination of Alternaria spp. habitats using 7-day volumetric spore trap, Hybrid Single Particle Lagrangian Integrated Trajectory model and geographic information system. Urban Climate,14, 429–440.CrossRefGoogle Scholar
  57. Ščevková, J., & Kováč, J. (2019). First fungal spore calendar for the atmosphere of Bratislava, Slovakia. Aerobiologia,35(2), 343–356.CrossRefGoogle Scholar
  58. Ščevková, J., Dušička, J., Mičieta, K., & Somorčík, J. (2016). The effects of recent changes in air temperature on trends in airborne Alternaria, Epicoccum and Stemphylium spore seasons in Bratislava (Slovakia). Aerobiologia,32(1), 69–81.CrossRefGoogle Scholar
  59. Şen, B., & Asan, A. (2001). Airborne fungi in vegetable growing areas of Edirne, Turkey. Aerobiologia,17(1), 69–75.CrossRefGoogle Scholar
  60. Simeray, J., Chaumont, J.-P., & Léger, D. (1993). Seasonal variations in the airborne fungal spore population of the East of France (Franche-Comte). Comparison between urban and rural environment during two years. Aerobiologia,9(2–3), 201–206.CrossRefGoogle Scholar
  61. Sindt, C., Besancenot, J.-P., & Thibaudon, M. (2016). Airborne Cladosporium fungal spores and climate change in France. Aerobiologia,32(1), 53–68.CrossRefGoogle Scholar
  62. Skjøth, C. A., Sommer, J., Brandt, J., Hvidberg, M., Geels, C., Hansen, K. M., et al. (2007). Copenhagen—a significant source of birch (Betula) pollen? International Journal of Biometeorology,52(6), 453.CrossRefGoogle Scholar
  63. Skjøth, C. A., Sommer, J., Frederiksen, L., & Gosewinkel Karlson, U. (2012). Crop harvest in Denmark and Central Europe contributes to the local load of airborne Alternaria spore concentrations in Copenhagen. Atmospheric Chemistry and Physics,12(22), 11107–11123.CrossRefGoogle Scholar
  64. Skjøth, C. A., Damialis, A., Belmonte, J., De Linares, C., Fernández-Rodríguez, S., Grinn-Gofroń, A., et al. (2016). Alternaria spores in the air across Europe: Abundance, seasonality and relationships with climate, meteorology and local environment. Aerobiologia,32(1), 3–22.CrossRefGoogle Scholar
  65. Smith, M., Jäger, S., Berger, U., Sikoparija, B., Hallsdottir, M., Sauliene, I., et al. (2014). Geographic and temporal variations in pollen exposure across Europe. Allergy,69, 913–923.CrossRefGoogle Scholar
  66. Sousa, L., Camacho, I. C., Grinn-Gofroń, A., & Camacho, R. (2016). Monitoring of anamorphic fungal spores in Madeira region (Portugal), 2003–2008. Aerobiologia,32(2), 303–315.CrossRefGoogle Scholar
  67. Stępalska, D., & Wołek, J. (2009). Intradiurnal periodicity of fungal spore concentrations (Alternaria, Botrytis, Cladosporium, Didymella, Ganoderma) in Cracow, Poland. Aerobiologia,25(4), 333.CrossRefGoogle Scholar
  68. Stieb, D. M., Beveridge, R. C., Brook, J. R., Smith-Doiron, M., Burnett, R. T., Dales, R. E., et al. (2000). Air pollution, aeroallergens and cardiorespiratory emergency department visits in Saint John, Canada. Journal of Exposure Science and Environmental Epidemiology,10(5), 461–477.CrossRefGoogle Scholar
  69. Twaroch, T. E., Curin, M., Valenta, R., & Swoboda, I. (2015). Mold allergens in respiratory allergy: from structure to therapy. Allergy Asthma Immunol Res,7(3), 205–220.CrossRefGoogle Scholar
  70. Ugolotti, M., Pasquarella, C., Vitali, P., Smith, M., & Albertini, R. (2015). Characteristics and trends of selected pollen seasons recorded in Parma (Northern Italy) from 1994 to 2011. Aerobiologia,31(3), 341–352.CrossRefGoogle Scholar
  71. Walther, G.-R. (2010). Community and ecosystem responses to recent climate change. Philosophical Transactions of the Royal Society B: Biological Sciences.,365, 2019–2024.CrossRefGoogle Scholar
  72. Weryszko-Chmielewska, E., Kasprzyk, I., Nowak, M., Sulborska, A., Kaczmarek, J., Szymanska, A., et al. (2018). Health hazards related to conidia of Cladosporium—Biological air pollutants in Poland, central Europe. Journal of Environmental Sciences,65, 271–281.CrossRefGoogle Scholar
  73. Zasada, I., Fertner, C., Piorr, A., & Nielsen, T. S. (2011). Peri-urbanisation and multifunctional adaptation of agriculture around Copenhagen AU—Zasada, Ingo. Geografisk Tidsskrift-Danish Journal of Geography,111(1), 59–72.CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Public HealthAarhus UniversityAarhusDenmark
  2. 2.School of Science and the EnvironmentUniversity of WorcesterWorcesterUK
  3. 3.Department of Environmental Science – Atmospheric EnvironmentAarhus UniversityRoskildeDenmark
  4. 4.The Asthma and Allergy AssociationRoskildeDenmark
  5. 5.Department of Environmental Science – Environmental Microbiology and Circular Resource FlowAarhus UniversityRoskildeDenmark

Personalised recommendations