Advertisement

Aerobiologia

, Volume 32, Issue 1, pp 3–22 | Cite as

Alternaria spores in the air across Europe: abundance, seasonality and relationships with climate, meteorology and local environment

  • C. A. Skjøth
  • A. Damialis
  • J. Belmonte
  • C. De Linares
  • S. Fernández-Rodríguez
  • A. Grinn-Gofroń
  • M. Jędryczka
  • I. Kasprzyk
  • D. Magyar
  • D. Myszkowska
  • G. Oliver
  • A. Páldy
  • C. H. Pashley
  • K. Rasmussen
  • J. Satchwell
  • M. Thibaudon
  • R. Tormo-Molina
  • D. Vokou
  • M. Ziemianin
  • M. Werner
OriginalPaper

Abstract

We explored the temporal and spatial variations in airborne Alternaria spore quantitative and phenological features in Europe using 23 sites with annual time series between 3 and 15 years. The study covers seven countries and four of the main biogeographical regions in Europe. The observations were obtained with Hirst-type spore traps providing time series with daily records. Site locations extend from Spain in the south to Denmark in the north and from England in the West to Poland in the East. The study is therefore the largest assessment ever carried out for Europe concerning Alternaria. Aerobiological data were investigated for temporal and spatial patterns in their start and peak season dates and their spore indices. Moreover, the effects of climate were checked using meteorological data for the same period, using a crop growth model. We found that local climate, vegetation patterns and management of landscape are governing parameters for the overall spore concentration, while the annual variations caused by weather are of secondary importance but should not be neglected. The start of the Alternaria spore season varies by several months in Europe, but the peak of the season is more synchronised in central-northern Europe in the middle of the summer, while many southern sites have peak dates either earlier or later than northern Europe. The use of a crop growth model to explain the start and peak of season suggests that such methods could be useful to describe Alternaria seasonality in areas with no available observations.

Keywords

Alternaria fungal spores Pathogens Aeroallergens Climate change Exposure 

Notes

Acknowledgments

Dr. C. A. Skjøth is supported by European Commission through a Marie Curie Career Integration Grant (Project ID CIG631745 and Acronym SUPREME). Dr. C. H. Pashley is supported by the Midlands Asthma and Allergy Research Association (MAARA) and the National Institute for Health Research Leicester Respiratory Biomedical Research Unit. Dr. S. Fernández-Rodríguez and Dr. R. Tormo-Molina are supported by Regional Government Science Foundation of the Junta de Extremadura through the two projects: PRI06A190, PRI BS10008. Dr. A. Damialis has been supported by the Research Committee of the Aristotle University of Thessaloniki (Excellence Fellowships of Postdoctoral Researchers, 2011). Dr. I. Kasprzyk and Dr. M. Jędryczkaare supported by National Science Centre Project No. N N305 321,737. The views expressed are those of the author(s) and not necessarily those of the European Commission, the NHS, the NIHR or the Department of Health.

Supplementary material

10453_2016_9426_MOESM1_ESM.pdf (36 kb)
Supplementary material 1 (PDF 35 kb)

References

  1. Agrios, G. N. (1997). Plant pathology. San Diego: Academic Press.Google Scholar
  2. Balkovic, J., van der Velde, M., Schmid, E., Skalsky, R., Khabarov, N., Obersteiner, M., et al. (2013). Pan-European crop modelling with EPIC: Implementation, up-scaling and regional crop yield validation. Agricultural Systems, 120, 61–75.CrossRefGoogle Scholar
  3. Beggs, P. J. (2004). Impacts of climate change on aeroallergens: Past and future. Clinical and Experimental Allergy, 34, 1507–1513.CrossRefGoogle Scholar
  4. Behbod, B., Sordillo, J. E., Hoffman, E. B., Datta, S., Webb, T. E., Kwan, D. L., et al. (2015). Asthma and allergy development: Contrasting influences of yeasts and other fungal exposures. Clinical and Experimental Allergy, 45, 154–163.CrossRefGoogle Scholar
  5. Berman, D. (2011). Climate change and aeroallergens in South Africa. Current Allergy and Clinical Immunology, 24, 65–71.Google Scholar
  6. Burbach, G. J., Heinzerling, L. M., Edenharter, G., Bachert, C., Bindslev-Jensen, C., Bonini, S., et al. (2009). GA(2)LEN skin test study II: clinical relevance of inhalant allergen sensitizations in Europe. Allergy, 64, 1507–1515.CrossRefGoogle Scholar
  7. Burshtein, N., Lang-Yona, N., & Rudich, Y. (2011). Ergosterol, arabitol and mannitol as tracers for biogenic aerosols in the eastern Mediterranean. Atmospheric Chemistry and Physics, 11, 829–839.CrossRefGoogle Scholar
  8. Bush, R. K., & Prochnau, J. J. (2004). Alternaria-induced asthma. Journal of Allergy and Clinical Immunology, 113, 227–234.CrossRefGoogle Scholar
  9. Cecchi, L., D’amato, G., Ayres, J. G., 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, 1073–1081.Google Scholar
  10. Cooter, E. J., Bash, J. O., Benson, V., & Ran, L. (2012). Linking agricultural crop management and air quality models for regional to national-scale nitrogen assessments. Biogeosciences, 9, 4023–4035.CrossRefGoogle Scholar
  11. 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, 191–199.CrossRefGoogle Scholar
  12. Crameri, R., Garbani, M., Rhyner, C., & Huitema, C. (2014). Fungi: The neglected allergenic sources. Allergy, 69, 176–185.CrossRefGoogle Scholar
  13. Dales, R. O. B. E., Cakmak, S. A. B. I., Burnett, R. I. C. H., Judek, S. T. A. N., Coates, F. R. A. N., & Brook, J. E. F. F. (2000). Influence of ambient fungal spores on emergency visits for asthma to a regional children’s hospital. American Journal of Respiratory and Critical Care Medicine, 162, 2087–2090.CrossRefGoogle Scholar
  14. Damialis, A., Mohammad, A., Halley, J., & Gange, A. (2015a). Fungi in a changing world: Growth rates will be elevated, but spore production may decrease in future climates. International Journal of Biometeorology, 59, 1157–1167.CrossRefGoogle Scholar
  15. 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
  16. De Linares, C., Belmonte, J., Canela, M., de la Guardia, C. D., Alba-Sanchez, F., Sabariego, S. A., & Nso-Perez, S. (2010). Dispersal patterns of Alternaria conidia in Spain. Agricultural and Forest Meteorology, 150, 1491–1500.CrossRefGoogle Scholar
  17. Deen, W., Swanton, C. J., & Hunt, L. A. (2001). A mechanistic growth and development model of common ragweed. Weed Science, 49, 723–731.CrossRefGoogle Scholar
  18. Denning, D. W., Pashley, C. H., Hartl, D., Wardlaw, A., Godet, C., Giacco, S. D., et al. (2014). Fungal allergy in asthma—state of the art and research needs. Clinical Biochemistry, 4, 1–23.Google Scholar
  19. Draxler, R., Stunder, B., Rolph, G., & Stein, A., & Taylor, A. (2014). Hysplit4 users guide. Revision September 2014. http://www.arl.noaa.gov/documents/reports/hysplit_user_guide.pdf.
  20. Dupuy, N. (2007). Lecture de spores fongiques. Technical Report, Reseau National de Surveillance Aerobiolique, Lyon.Google Scholar
  21. Escuredo, O., Seijo, M., Fernández-González, M., & Iglesias, I. (2011). Effects of meteorological factors on the levels of Alternaria spores on a potato crop. International Journal of Biometeorology, 55, 243–252.CrossRefGoogle Scholar
  22. European Commission. (2005). Image2000 and CLC2000 products and methods. European Commission, Joint Research Center (DG JRC), Institute for Environment and Sustainability, Land Management Unit, I-21020 Ispra, VA.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. Friesen, T. L., De Wolf, E. D., & Francl, L. J. (2001). Source strength of wheat pathogens during combine harvest. Aerobiologia, 17, 293–299.CrossRefGoogle Scholar
  25. Galán, C., Smith, M., Thibaudon, M., Frenguelli, G., Oteros, J., Gehrig, R., et al. (2014). Pollen monitoring: Minimum requirements and reproducibility of analysis. Aerobiologia, 30, 385–395.CrossRefGoogle Scholar
  26. Gioulekas, D., Damialis, A., Papakosta, D., Spieksma, F., Giouleka, P., & Patakas, D. (2004). Allergenic fungi spore records (15 years) and sensitization in patients with respiratory allergy in Thessaloniki-Greece. J Invest Allergo Clin Imm, 14, 225–231.Google Scholar
  27. Gravesen, S. (1979). Fungi as a cause of allergic disease. Allergy, 34, 135–154.CrossRefGoogle Scholar
  28. Gravesen, S., Frisvad, J. C., & Samson, R. A. (1994). Microfungi: Munksgaard. Copenhagen: Denmark. ISBN 9788716114365.Google Scholar
  29. Grewling, Ł., Šikoparija, B., Skjøth, C. A., Radišić, P., Apatini, D., Magyar, D., et al. (2012). Variation in Artemisia pollen seasons in Central and Eastern Europe. Agricultural and Forest Meteorology, 160, 48–59.CrossRefGoogle Scholar
  30. Grinn-Gofron, A., & Strzelczak, A. (2008). Artificial neural network models of relationships between Alternaria spores and meteorological factors in Szczecin (Poland). International Journal of Biometeorology, 52, 859–868.CrossRefGoogle Scholar
  31. Gundel, P. E., Garibaldi, L. A., Helander, M., & Saikkonen, K. (2013). Symbiotic interactions as drivers of trade-offs in plants: Effects of fungal endophytes on tall fescue. Fungal Diversity, 60, 5–14.CrossRefGoogle Scholar
  32. Gyldenkærne, S., Ambelas Skjøth, C., Hertel, O., & Ellermann, T. (2005). A dynamical ammonia emission parameterization for use in air pollution models. Journal Geophysical Research, 110, 1–14. doi: 10.1029/2004JD005459.CrossRefGoogle Scholar
  33. Hatzipapas, P., Kaloskak, K., Dara, A., & Christias, C. (2002). Spore germination and appressorium formation in the entomopathogenic Alternaria alternata. Mycological Research, 106(11), 1349–1359.CrossRefGoogle Scholar
  34. Hauptman, T., Pitcairn, C. E. R., de Groot, M., Ogris, N., Ferlan, M., & Jurc, D. (2013). Temperature effect on Chalara fraxinea: Heat treatment of saplings as a possible disease control method. Forest Pathology, 43, 360–370.Google Scholar
  35. Helfer, S. (2014). Rust fungi and global change. New Phytologist, 201, 770–780.CrossRefGoogle Scholar
  36. Hirst, J. M. (1952). An automatic volumetric spore trap. Annals of Applied Biology, 39, 257–265.CrossRefGoogle Scholar
  37. Hoose, C., & Möhler, O. (2012). Heterogeneous ice nucleation on atmospheric aerosols: A review of results from laboratory experiments. Atmospheric Chemistry and Physics Discussions, 12, 12531–12621.CrossRefGoogle Scholar
  38. Iglesias, I., Rodríguez-Rajo, F., & Méndez, J. (2007). Evaluation of the different Alternaria prediction models on a potato crop in A Limia (NW of Spain). Aerobiologia, 23, 27–34.CrossRefGoogle Scholar
  39. Käpyla, M., & Penttinen, A. (1981). An evaluation of the microscopial counting methods of the tape in Hirst–Burkard pollen and spore trap. Grana, 20, 131–141.CrossRefGoogle Scholar
  40. Karrer, G., Skjøth, C. A., Šikoparija, B., Smith, M., Berger, U., & Essl, F. (2015). Ragweed (Ambrosia) pollen source inventory for Austria. Science of the Total Environment, 523, 120–128.CrossRefGoogle Scholar
  41. Kasprzyk, I., Rodinkova, V., Sauliene, I., Ritenberga, O., Grinn-Gofron, A., Nowak, M., et al. (2015). Air pollution by allergenic spores of the genus Alternaria in the air of central and eastern Europe. Environmental Science and Pollution Research, 22, 9260–9274.CrossRefGoogle Scholar
  42. Kasprzyk, I., & Worek, M. (2006). Airborne fungal spores in urban and rural environments in Poland. Aerobiologia, 22, 169–176.CrossRefGoogle Scholar
  43. Kirtman, B., Power, S. B., Adedovin, J. A., Boer, G. J., Bojarju, R., Camiloni, I., et al. (2013). Near-term climate change: Projections and predictability. In T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, & P. M. Midgley (Eds.), Climate Change 2013: The physical science basis. Contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press.Google Scholar
  44. Knutsen, A. P., Bush, R. K., Demain, J. G., Denning, D. W., Dixit, A., Fairs, A., et al. (2012). Fungi and allergic lower respiratory tract diseases. Journal of Allergy and Clinical Immunology, 129, 280–291.CrossRefGoogle Scholar
  45. Makra, L., Santa, T., Matyasovszky, I., Damialis, A., Karatzas, K., Bergmann, K. C., et al. (2010). Airborne pollen in three European cities: Detection of atmospheric circulation pathways by applying three-dimensional clustering of backward trajectories. Journal Geophysical Research. doi: 10.1029/2010JD014743.Google Scholar
  46. Mari, A., Schneider, P., Wally, V., Breitenbach, M., & Simon-Nobbe, B. (2003). Sensitization to fungi: Epidemiology, comparative skin tests, and IgE reactivity of fungal extracts. Clinical and Experimental Allergy, 33, 1429–1438.CrossRefGoogle Scholar
  47. Maya-Manzano, J., Fernández-Rodriguez, S., Hernández-Trejo, F., Díaz-Peres, G., Gonzalo-Garijo, Á., Silva-Palacios, I., et al. (2012). Seasonal Mediterranean pattern for airborne spores of Alternaria. Aerobiologia, 28, 515–525.CrossRefGoogle Scholar
  48. McMaster, G. S., & Wilhelm, W. W. (1997). Growing degree-days: One equation, two interpretations. Agricultural and Forest Meteorology, 87, 291–300.CrossRefGoogle Scholar
  49. Nilsson, S., & Persson, S. (1981). Tree pollen spectra in the Stockholm region (Sweden), 1973–1980. Grana, 20, 179–182.CrossRefGoogle Scholar
  50. Oerke, E. C., & Dehne, H. W. (2004). Safeguarding production-losses in major crops and the role of crop protection. Crop Protection, 23, 275–285.CrossRefGoogle Scholar
  51. Olesen, J. E., & Plauborg, F. (1995). MVTOOL version 1.10 for developing MARKVAND. SP Rep. 27, Danish Institute of Plant and Soil Science, Tjele.Google Scholar
  52. Paldy, A., Bobvos, J., Fazekas, B., Manyoki, G., Malnasi, T., & Magyar, D. (2014). Characterisation of the pollen season by using climate specific pollen indicators. Central European Journal of Occupational and Environmental Medicine, 20, 199–214.Google Scholar
  53. Pashley, C., Fairs, A., Edwards, R., Bailey, J., Corden, J., & Wardlaw, A. (2009). Reproducibility between counts of airborne allergenic pollen from two cities in the East Midlands, UK. Aerobiologia, 25, 249–263.CrossRefGoogle Scholar
  54. Poorter, H., van de Vijver, C. A. D. M., Boot, R. G. A., & Lambers, H. (1995). Growth and carbon economy of a fast-growing and a slow-growing grass species as dependent on nitrate supply. Pland and Soil, 171(2), 217–227.CrossRefGoogle Scholar
  55. Sadyś, M., Skjøth, C. A., & Kennedy, R. (2014). Back-trajectories show export of airborne fungal spores (Ganoderma sp.) from forests to agricultural and urban areas in England. Atmospheric Environment, 84, 88–99.CrossRefGoogle 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. Seifert, K., Morgan-Jones, G., Gams, W., & Kendrick, B. (2011). The genera of hyphomycetes. CBS Biodiversity Series no. 9: 1–997, CBS-KNAW Fungal Biodiversity Centre, Utrecht.Google Scholar
  58. Šikoparija, B., Pejak-Šikoparija, T., Radišić, P., Smith, M., & Soldevilla, C. G. (2011). The effect of changes to the method of estimating the pollen count from aerobiological samples. Journal of Environmental Monitoring, 13, 384–390.CrossRefGoogle Scholar
  59. Simmons, E. G. (2007). Alternaria. An identification manual (1st ed.). CBS Biodiversity Series. UtrechtGoogle Scholar
  60. Skjøth, C. A., Baker, P., Sadyś, M., & Adams-Groom, B. (2015). Adams-Groom B. (2015). Pollen from alder (Alnus sp.), birch (Betula sp.) and oak (Quercus sp.) in the UK originate from small woodlands. Urban Climate, 14, 414–428.CrossRefGoogle Scholar
  61. Skjøth, C. A., Smith, M., Šikoparija, B., Stach, A., Myszkowska, D., Kasprzyk, I., et al. (2010). A method for producing airborne pollen source inventories: An example of Ambrosia (ragweed) on the Pannonian Plain. Agricultural and Forest Meteorology, 150, 1203–1210.CrossRefGoogle Scholar
  62. 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, 11107–11123.CrossRefGoogle Scholar
  63. Smith, M., Jäger, S., Berger, U., Šikoparija, B., Hallsdottir, M., Sauliene, I., et al. (2014). Geographic and temporal variations in pollen exposure across Europe. Allergy, 69, 913–923.CrossRefGoogle Scholar
  64. Smith, M., Skjøth, C. A., Myszkowska, D., Uruska, A., Malgorzata, P., Stach, A., et al. (2008). Long-range transport of Ambrosia pollen to Poland. Agricultural and Forest Meteorology, 148, 1402–1411.CrossRefGoogle Scholar
  65. Stepalska, D., & Wolek, J. (2009). Intradiurnal periodicity of fungal spore concentrations (Alternaria, Botrytis, Cladosporium, Didymella, Ganoderma) in Cracow, Poland. Aerobiologia, 25, 333–340.CrossRefGoogle Scholar
  66. Su’udi, M., J-M, Park, Park, S. R., Hwang, D. J., Bae, D. J., Kim, S., & Ahn, I. P. (2013). Quantification of Alternaria brassicicola infection in the Arabidopsis thaliana and Brassica rapa subsp. pekinensis. Microbiology, 159, 1946–1955.CrossRefGoogle Scholar
  67. Suzuki, R. (2014) Hierarchical clustreing with p values via multiscale bootstrap resampling. CRAN.Google Scholar
  68. Suzuki, R., & Shimodaira, H. (2006). Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics, 22, 1540–1542.CrossRefGoogle Scholar
  69. R Core Team and Contributors Worldwide. (2015). The R Stats Package. https://stat.ethz.ch/R-manual/R-patched/library/stats/html/00Index.html.
  70. TheLancet. (2008). Allergic rhinitis: Common, costly, and neglected. The Lancet, 371, 2057.CrossRefGoogle Scholar
  71. Thibaudon, M., Šikoparija, B., Oliver, G., Smith, M., & Skjøth, C. A. (2014). Ragweed pollen source inventory for France—the second largest centre of Ambrosia in Europe. Atmospheric Environment, 83, 62–71.CrossRefGoogle Scholar
  72. Toth, B., Csosz, M., Szabo-Hever, A., Simmons, E. G., Samson, R. A., & Varga, J. (2011). Alternaria hungarica sp., a minor foliar pathogen of wheat in Hungary. Mycologia, 103, 94–100.CrossRefGoogle Scholar
  73. Zhang, Y., Bielory, L., Cai, T., Mi, Z., & Georgopoulos, P. (2015). Predicting onset and duration of airborne allergenic pollen season in the United States. Atmospheric Environment, 103, 297–306.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • C. A. Skjøth
    • 1
  • A. Damialis
    • 2
  • J. Belmonte
    • 3
    • 4
  • C. De Linares
    • 3
    • 4
  • S. Fernández-Rodríguez
    • 5
  • A. Grinn-Gofroń
    • 6
  • M. Jędryczka
    • 7
  • I. Kasprzyk
    • 8
  • D. Magyar
    • 9
  • D. Myszkowska
    • 10
  • G. Oliver
    • 11
  • A. Páldy
    • 9
  • C. H. Pashley
    • 12
  • K. Rasmussen
    • 13
  • J. Satchwell
    • 12
  • M. Thibaudon
    • 11
  • R. Tormo-Molina
    • 14
  • D. Vokou
    • 2
  • M. Ziemianin
    • 10
  • M. Werner
    • 1
  1. 1.National Pollen and Aerobiology Research Unit, Institute of Science and the EnvironmentUniversity of WorcesterWorcesterUK
  2. 2.Department of Ecology, School of BiologyAristotle University of ThessalonikiThessaloníkiGreece
  3. 3.Institute for Environmental Sciences and Technology (ICTA-UAB)Universitat Autònoma de BarcelonaCerdanyola del VallèsSpain
  4. 4.Department of Animal Biology, Plant Biology and Ecology, Faculty of BiosciencesUniversitat Autònoma de BarcelonaCerdanyola del VallèsSpain
  5. 5.Department of Construction, Polythecnic SchoolUniversity of ExtremaduraExtremaduraSpain
  6. 6.Department of Plant Taxonomy and PhytogeographyUniversity of SzczecinSzczecinPoland
  7. 7.Institute of Plant GeneticPolish Academy of SciencePoznańPoland
  8. 8.Department of Environmental BiologyUniversity of RzeszówRzeszówPoland
  9. 9.National Public Health CenterBudapestHungary
  10. 10.Department of Clinical and Environmental AllergologyJagiellonian University Medical CollegeKrakówPoland
  11. 11.Reseau National de Surveillance Aerobiologique (RNSA)BrussieuFrance
  12. 12.Aerobiology Unit, Institute for Lung Health, Department of Infection, Immunity and InflammationUniversity of LeicesterLeicesterUK
  13. 13.The Asthma and Allergy AssociationRoskildeDenmark
  14. 14.Department of Plant Biology, Ecology and Earth Sciences, Faculty of ScienceUniversity of ExtremaduraExtremaduraSpain

Personalised recommendations