Aerobiologia

, Volume 32, Issue 1, pp 53–68 | Cite as

Airborne Cladosporium fungal spores and climate change in France

  • Charlotte Sindt
  • Jean-Pierre Besancenot
  • Michel Thibaudon
Original Paper

Abstract

Fungal spores are among the most commonly encountered airborne biological particles, and it is widely proved that they represent a potential source of allergens involved in rhinitis and asthma. A change in temperature may influence the colonisation and growth of fungi directly through the physiology of individual organisms, or indirectly through physiological effects on their host plants or substrates and any competitors or enemies. In order to detect and monitor the evolution of the spore counts, air sampling was carried out using standard equipment (Hirst-type volumetric traps) and an identical method in several stations across France. Cladosporium has been here emphasised because of its very large contribution to the total fungal spectrum. Moreover, this taxon is of particular clinical importance because it possesses a high allergenic potential. The data from the oldest traps (Aix-en-Provence, Bordeaux, Lyon, Paris and Toulouse) were analysed on an annual base. Located at different latitudes and in different climatic areas, these five cities showed fundamentally different trends for the concentrations of Cladosporium spores: downward trend at the southernmost locations and upward trend at the other locations, whereas temperature was everywhere continuously rising over the study period. However, longer data sets are needed to be able to draw more definitive conclusions about quantitative trends in airborne fungal spore concentrations.

Keywords

Aerobiology Annual fungal spore record Cladosporium Trend analysis Temperature France 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adams, K. F. (1964). Year to year variation in the fungus spore content of the atmosphere. Acta Allergologica, 19(1), 11–50. doi: 10.1111/j.1398-9995.1964.tb03220.x.CrossRefGoogle Scholar
  2. 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. doi: 10.1080/00173134.2012.717636.CrossRefGoogle Scholar
  3. Aira, M. J., Rodríguez-Rajo, F. J., & Jato, V. (2008). 47 annual records of allergenic fungi spore: Predictive models from the NW Iberian Peninsula. Annals of Agricultural and Environmental Medicine, 15(1), 91–98.Google Scholar
  4. Aukrust, L. (1979). Crossed radioimmunoelectrophoretic studies of distinct allergens in two extracts of Cladosporium herbarum. International Archives of Allergy and Applied Immunology, 58(4), 375–390. doi: 10.1159/000232217.CrossRefGoogle Scholar
  5. Bagni, B., Davies, R. R., Mallea, M., Nolard, N., Spieksma, F. T., & Stix, E. (1977). Sporenkonzentrationen in Städten der Europäischen Gemeinschaft (EG). II. Cladosporium- und Alternaria-Sporen. Acta Allergologica, 32(2), 118–138. doi: 10.1111/j.1398-9995.1977.tb02617.x.CrossRefGoogle Scholar
  6. Barnes, C. S., Alexis, N. E., Bernstein, J. A., Cohn, J. R., Demain, J. G., Horner, E., et al. (2013). Climate change and our environment: The effect on respiratory and allergic disease. Journal of Allergy and Clinical Immunology: In Practice, 1(2), 137–141. doi: 10.1016/j.jaip.2012.07.002.CrossRefGoogle Scholar
  7. Beggs, P. J. (2004). Impacts of climate change on aeroallergens: Past and future. Clinical and Experimental Allergy, 34(10), 1507–1513. doi: 10.1111/j.1365-2222.2004.02061.x.CrossRefGoogle Scholar
  8. Bensch, K., Braun, U., Groenewald, J. Z., & Crous, P. W. (2012). The genus Cladosporium. Studies in Mycology, 72(1), 1–401. doi: 10.3114/sim0003.CrossRefGoogle Scholar
  9. Besancenot, J. P., & Thibaudon, M. (2012). Changement climatique et pollinisation. Revue des Maladies Respiratoires, 29(10), 1238–1253. doi: 10.1016/j.rmr.2012.07.007.CrossRefGoogle Scholar
  10. Bousquet, P. J., Chinn, S., Janson, C., Kogevinas, M., Burney, P., & Jarvis, D. (2007). Geographical variation in the prevalence of positive skin tests to environmental aeroallergens in the European Community Respiratory Health Survey I. Allergy, 62(3), 301–309. doi: 10.1111/j.1398-9995.2006.01293.x.CrossRefGoogle Scholar
  11. 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(9), 1073–1081. doi: 10.1111/j.1398-9995.2010.02423.x.Google Scholar
  12. 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. doi: 10.1023/A:1010876917512.CrossRefGoogle Scholar
  13. Corden, J. M., Millington, W. M., & Mulllins, 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), 191–199. doi: 10.1023/B:AERO.0000006529.51252.2f.CrossRefGoogle Scholar
  14. Damialis, A., Halley, J. M., Gioulekas, D., & Vokou, D. (2007). Long-term trends in atmospheric pollen levels in the city of Thessaloniki, Greece. Atmospheric Environment, 41(33), 7011–7021. doi: 10.1016/j.atmosenv.2007.05.009.CrossRefGoogle Scholar
  15. 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. doi: 10.1007/s00484-014-0927-0.CrossRefGoogle Scholar
  16. 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. doi: 10.1016/j.funeco.2014.09.010.CrossRefGoogle Scholar
  17. Dugan, F. M., Schubert, K., & Braun, U. (2004). Check-list of Cladosporium names. Schlechtendalia, 11, 1–103.Google Scholar
  18. Estienne, P. (1979). La France, I. Généralités, Région du Nord. Paris: Masson.Google Scholar
  19. Fukutomi, Y., & Taniguchi, M. (2015). Sensitization to fungal allergens: Resolved and unresolved issues. Allergology International, 64(4), 321–331. doi: 10.1016/j.alit.2015.05.007.CrossRefGoogle Scholar
  20. Gobakken, L. R. (2010). Effects of global climate change on mould growth—Interactions of concern. In 41 st Annual Meeting of the International Research Group on Wood Protection, Biarritz, 9–13 May 2010 (pp. 1–11). Stockholm: IRG Secretariat.Google Scholar
  21. Goodman, D. H., Northey, W. T., Leathers, C. R., & Savage, T. H. (1966). A study of airborne fungi in the Phoenix, Arizona, metropolitan area. Journal of Allergy, 38(1), 56–62. doi: 10.1016/0021-8707(66)90074-8.CrossRefGoogle Scholar
  22. Gravesen, S. (1979). Fungi as a cause of allergic disease. Allergy, 34(3), 135–154. doi: 10.1111/j.1398-9995.1979.tb01562.x.CrossRefGoogle Scholar
  23. Grinn-Gofroń, A. (2009). The occurrence of Cladosporium spores in the air and their relationships with meteorological parameters. Acta Agrobotanica, 62(2), 111–116. doi: 10.5586/aa.2009.032.CrossRefGoogle Scholar
  24. Grinn-Gofroń, A., & Bosiacka, B. (2015). Effects of meteorological factors on the composition of selected fungal spores in the air. Aerobiologia, 31(1), 63–72. doi: 10.1007/s10453-014-9347-1.CrossRefGoogle Scholar
  25. Grinn-Gofroń, A., & Rapiejko, P. (2009). Occurrence of Cladosporium spp. and Alternaria spp. spores in Western, Northern and Central-Eastern Poland in 2004–2006 and relation to some meteorological factors. Atmospheric Research, 93(4), 747–758. doi: 10.1016/j.atmosres.2009.02.014.CrossRefGoogle Scholar
  26. Grinn-Gofroń, A., & Strzelczak, A. (2008). Artificial neural network models of relationships between Cladosporium spores and meteorological factors in Szczecin (Poland). Grana, 47(4), 305–315. doi: 10.1080/00173130802513784.CrossRefGoogle Scholar
  27. Hamilos, D. L. (2010). Allergic fungal rhinitis and rhinosinusitis. Proceedings of the American Thoracic Society, 7(3), 245–252. doi: 10.1513/pats.200909-098AL.CrossRefGoogle Scholar
  28. Hansen, J., Sato, M., Ruedy, R., Lo, K., Lea, D. W., & Medina-Elizade, M. (2006). Global temperature change. Proceedings of the National Academy of Sciences, 103(39), 14288–14293. doi: 10.1073/pnas.0606291103.CrossRefGoogle Scholar
  29. Herrero, B., & Zaldivar, P. (1997). Effects of meteorological factors on the levels of Alternaria and Cladosporium spores in the atmosphere of Palencia, 1990–1992. Grana, 36(3), 180–184. doi: 10.1080/00173139709362606.CrossRefGoogle Scholar
  30. Hirst, J. M. (1952). An automatic volumetric spore trap. Annals of Applied Biology, 39(2), 257–265. doi: 10.1111/j.1744-7348.1952.tb00904.x.CrossRefGoogle Scholar
  31. Hjelmroos, M. (1993). Relationship between airborne fungal spore presence and weather variables: Cladosporium and Alternaria. Grana, 32(1), 40–47. doi: 10.1080/00173139309436418.CrossRefGoogle Scholar
  32. Ho, H. M., Rao, C. Y., Hsu, H. H., Chiu, Y. H., Liu, C. M., & Chao, H. J. (2005). Characteristics and determinants of ambient fungal spores in Hualien, Taiwan. Atmospheric Environment, 39(32), 5839–5850. doi: 10.1016/j.atmosenv.2005.06.034.CrossRefGoogle Scholar
  33. Hollins, P. D., Kettlewell, P. S., Atkinson, M. D., Stephenson, D. B., Corden, J. M., Millington, W. M., 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. doi: 10.1007/s00484-003-0188-9.CrossRefGoogle Scholar
  34. Hyde, K. D., McKenzie, E. H. C., & KoKo, T. W. (2011). Towards incorporating anamorphic fungi in a natural classification—Checklist and notes for 2010. Mycosphere, 2(1), 1–88.Google Scholar
  35. Käpylä, M., & Penttinen, A. (1981). An evaluation of the microscopal counting methods of the tape in Hirst-Burkard pollen and spore trap. Grana, 20(2), 131–141. doi: 10.1080/00173138109427653.CrossRefGoogle Scholar
  36. Kasprzyk, I., Rodinkova, V., Šaulienė, I., Ritenberga, O., Grinn-Gofroń, 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(12), 9260–9274. doi: 10.1007/s11356-014-4070-6.CrossRefGoogle Scholar
  37. Katial, R. K., Zhang, Y., Jones, R. H., & Dyer, P. D. (1997). Atmospheric mold spore counts in relation to meteorological parameters. International Journal of Biometeorology, 41(1), 17–22. doi: 10.1007/s004840050048.CrossRefGoogle Scholar
  38. Kinney, P. L. (2008). Climate change, air quality, and human health. American Journal of Preventive Medicine, 35(5), 459–467. doi: 10.1016/j.amepre.2008.08.025.CrossRefGoogle Scholar
  39. Kurkela, T. (1997). The number of Cladosporium conidia in the air in different weather conditions. Grana, 36(1), 54–61. doi: 10.1080/00173139709362591.CrossRefGoogle Scholar
  40. Lavaud, F., & Dutau, G. (2013). Spores fongiques atmosphériques et allergies respiratoires. Revue Française d’Allergologie et d’Immunologie Clinique, 53(7), 567–568. doi: 10.1016/j.reval.2013.10.003.CrossRefGoogle Scholar
  41. Limpert, E., Burke, J., Galán, C., del Mar Trigo, M., West, J. S., & Stahel, W. A. (2008). Data, not only in aerobiology: How normal is the normal distribution? Aerobiologia, 24(3), 121–124. doi: 10.1007/s10453-008-9092-4.CrossRefGoogle Scholar
  42. Malling, H. J., Dreborg, S., & Weeke, B. (1987). Diagnosis and immunotherapy of mould allergy, part VI. Allergy, 42(4), 305–314. doi: 10.1111/j.1398-9995.1987.tb02214.x.CrossRefGoogle Scholar
  43. Mitakakis, T. Z., & Guest, D. I. (2001). A fungal spore calendar for the atmosphere of Melbourne, Australia, for the year 1993. Aerobiologia, 17(2), 171–176. doi: 10.1023/A:1011028412526.CrossRefGoogle Scholar
  44. Mitakakis, T. Z., & McGee, P. A. (2000). Reliability of measures of spores of Alternaria and pollen concentrations in air over two towns in rural Australia. Multiple sites for Burkard sampling. Grana, 39(2–3), 141–145. doi: 10.1080/001731300300045300.CrossRefGoogle Scholar
  45. Money, N. P. (2015). Spore production, discharge and dispersal. In S. C. Watkinson, L. Boddy, & N. P. Money (Eds.), The Fungi (3rd ed., pp. 67–97). London: Academic Press.Google Scholar
  46. Mullins, J. (2001). Microorganisms in outdoor air. In B. Flannigan, R. A. Samson, & J. D. Miller (Eds.), Microorganisms in home and indoor work environments: Diversity, health impacts, investigation and control (pp. 3–16). London: Taylor & Francis.Google Scholar
  47. Newnham, R. M. (1999). Monitoring biogeographical response to climate change: The potential role of aeropalynology. Aerobiologia, 15(2), 87–94. doi: 10.1023/A:1007595615115.CrossRefGoogle Scholar
  48. Nilsson, S., & Persson, S. (1981). Tree pollen spectra in the Stockholm region (Sweden), 1973–1980. Grana, 20(3), 179–182. doi: 10.1080/00173138109427661.CrossRefGoogle Scholar
  49. Nogales, M. T., Galán Soldevilla, C., Ruíz de Clavijo, J. E., & Dominguez Vilches, E. (1985). Variación estacional del contenido de esporas de Cladosporium en la atmósfera de Córdoba. Anales de la Asociación de Palinólogos de Lengua Española, 2, 339–345.Google Scholar
  50. O’Connor, D. J., Sadyś, M., Skjøth, C. A., 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. doi: 10.1007/s10453-014-9337-3.CrossRefGoogle Scholar
  51. Oliveira, M., Ribeiro, H., Delgado, L., & Abreu, I. (2009). The effects of meteorological factors on airborne fungal spore concentration in two areas differing in urbanization level. International Journal of Biometeorology, 53(1), 61–73. doi: 10.1007/s00484-008-0191-2.CrossRefGoogle Scholar
  52. Pidek, I. A., Poska, A., & Kaszewski, B. M. (2015). Taxon-specific pollen deposition dynamics in a temperate forest zone, SE Poland: The impact of physiological rhythmicity and weather controls. Aerobiologia, 31(2), 219–238. doi: 10.1007/s10453-014-9359-x.CrossRefGoogle Scholar
  53. Pringle, A. (2013). Asthma and the diversity of fungal spores in air. PLoS Pathogens, 9(6), e1003371. doi: 10.1371/journal.ppat.1003371.CrossRefGoogle Scholar
  54. Rapiejko, P., Stanlaewicz, W., Szczygielski, K., & Jurkiewicz, D. (2007). Progowe stężenie pyłku roślin niezbędne do wywołania objawów alergicznych/Threshold pollen count necessary to evoke allergic symptoms. Otolaryngologia Polska, 61(4), 591–594.CrossRefGoogle Scholar
  55. Recio, M., del Mar Trigo, M., Docampo, S., Melgar, M., García-Sánchez, J., Bootello, L., et al. (2012). Analysis of the predicting variables for daily and weekly fluctuations of two airborne fungal spores: Alternaria and Cladosporium. International Journal of Biometeorology, 56(6), 983–991. doi: 10.1007/s00484-011-0509-3.CrossRefGoogle Scholar
  56. 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. doi: 10.1017/S0953756204001777.CrossRefGoogle Scholar
  57. Sabariego, S., Díaz de la Guarda, C., & Alba, F. (2000). The effect of meteorological factors on the daily variation of airborne fungal spores in Granada (Southern Spain). International Journal of Biometeorology, 44(1), 1–5. doi: 10.1007/s004840050131.CrossRefGoogle Scholar
  58. Sadyś, M., Kennedy, R., & West, J. S. (2015a). Potential impact of climate change on fungal distributions: Analysis of 2 years of contrasting weather in the UK. Aerobiologia,. doi: 10.1007/s10453-015-9402-6.Google Scholar
  59. Sadyś, M., Strzelczak, A., Grinn-Gofroń, A., & Kennedy, R. (2015b). Application of redundancy analysis for aerobiological data. International Journal of Biometeorology, 59(1), 25–36. doi: 10.1007/s00484-014-0818-4.CrossRefGoogle Scholar
  60. Shapiro, S. S., & Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). Biometrika, 52(3–4), 591–611. doi: 10.2307/2333709.CrossRefGoogle Scholar
  61. Shelton, B. G., Kirkland, K. H., Flanders, W. D., & Morris, G. K. (2002). Profiles of airborne fungi in buildings and outdoor environments in the United States. Applied and Environmental Microbiology, 68(4), 1743–1753. doi: 10.1128/AEM.68.4.1743-1753.2002.CrossRefGoogle Scholar
  62. 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(7), 913–923. doi: 10.1111/all.12419.CrossRefGoogle Scholar
  63. Spieksma, F. T. M., Corden, J. M., Detandt, M., Millington, W. M., Nikkels, H., Nolard, N., et al. (2003). Quantitative trends in annual totals of five common airborne pollen types (Betula, Quercus, Poaceae, Urtica, and Artemisia), at five pollen-monitoring stations in Western Europe. Aerobiologia, 19(3), 171–184. doi: 10.1023/B:AERO.0000006528.37447.15.CrossRefGoogle Scholar
  64. Stępalska, D., Harmata, K., Kasprzyk, I., Myszkowska, D., & Stach, A. (1999). Occurrence of airborne Cladosporium and Alternaria spores in Southern and Central Poland in 1995–1996. Aerobiologia, 15(1), 39–47. doi: 10.1023/A:1007536513836.CrossRefGoogle Scholar
  65. Stępalska, D., & Wołek, J. (2005). Variation in fungal spore concentrations of selected taxa associated to weather conditions in Cracow, Poland, in 1997. Aerobiologia, 21(1), 43–52. doi: 10.1007/s10453-004-5877-2.CrossRefGoogle Scholar
  66. Thibaudon, M., & Lachasse, C. (2006). Alternaria, Cladosporium: Dispersion atmosphérique, rythmes nycthéméral et saisonnier. Revue Française d’Allergologie et d’Immunologie Clinique, 46(3), 188–196. doi: 10.1016/j.allerg.2006.01.025.CrossRefGoogle Scholar
  67. 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. doi: 10.1007/s10453-015-9368-4.CrossRefGoogle Scholar
  68. Valencia-Barrera, R. M., Comtois, P., & Fernández-González, D. (2002). Bioclimatic indices as a tool in pollen forecasting. International Journal of Biometeorology, 46(4), 171–175. doi: 10.1007/s00484-002-0138-y.CrossRefGoogle Scholar
  69. Vélez-Pereira, A. M., De Linares, C., Delgado, R., & Belmonte, J. (2015). Temporal trends of the airborne fungal spores in Catalonia (NE Spain), 1995–2013. Aerobiologia. 1–15. doi:  10.1007/s10453-015-9410-6.
  70. Ziello, C., Sparks, T. H., Estrella, N., Belmonte, J., Bergmann, K. C., Bucher, E., et al. (2012). Changes to airborne pollen counts across Europe. PLoS One, 7(4), e34076. doi: 10.1371/journal.pone.0034076.

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Charlotte Sindt
    • 1
  • Jean-Pierre Besancenot
    • 1
  • Michel Thibaudon
    • 1
  1. 1.Réseau National de Surveillance AérobiologiqueBrussieuFrance

Personalised recommendations