Ice nucleation by fungal spores from the classes agaricomycetes, ustilaginomycetes, and eurotiomycetes, and the effect on the atmospheric transport of these spores

Atmospheric Chemistry and Physics

Volumn 14, Issue 16, 2014, Pages 8611-8630

  Haga, D I ^a   Burrows, S M ^b   Iannone, R ^a,d   Wheeler, M J ^a   Mason, R H ^a   Chen, J ^a   Polishchuk, E A ^a   Poschl U ^c   Bertram, A K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^c MAX PLANCK INSTITUTE FOR CHEMISTRY   (Germany)

^d ENVIRONMENT CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGY; ATMOSPHERIC TRANSPORT; CLOUD CONDENSATION NUCLEUS; CONCENTRATION (COMPOSITION); DUST; FUNGUS; PATHOGEN; SCAVENGING (CHEMISTRY); SPORE; TROPOSPHERE;

ASCOMYCOTA; BASIDIOMYCOTA; EUROTIOMYCETES; USTILAGINOMYCETES;

EID: 84906675409     PISSN: 16807316     EISSN: 16807324     Source Type: Journal    
DOI: 10.5194/acp-14-8611-2014     Document Type: Article

References (133)

1. Aghedo, A. M., Rast, S., and Schultz, M. G.: Sensitivity of tracer transport to model resolution, prescribed meteorology and tracer lifetime in the general circulation model ECHAM5, Atmos. Chem. Phys., 10, 3385-3396, doi:10.5194/acp-10-3385-2010, 2010.
2. Allan, E. J. and Prosser, J. I.: Mycelial growth and branching of Streptomyces coelicolor A3(2) on solid medium, J. Gen. Microbiol., 129, 2029-2036, 1983.
3. Amato, P., Parazols, M., Sancelme, M., Laj, P., Mailhot, G., and Delort, A. M.: Microorganisms isolated from the water phase of tropospheric clouds at the Puy de Dôme: major groups and growth abilities at low temperatures, FEMS Microbiol. Ecol., 59, 242-254, doi:10.1111/j.1574-6941.2006.00199.x, 2007. (Pubitemid 46105865)
4. Andrade, D., Pan, Z., Dannevik, W., and Zidek, J.: Modeling soybean rust spore escape from infected canopies: model description and preliminary results, J. Appl. Meteorol., 48, 789-803, doi:10.1175/2008jamc1917.1, 2009.
5. Anikster, Y., Szabo, L. J., Eilam, T., Manisterski, J., Koike, S. T., and Bushnell, W. R.: Morphology, life cycle biology, and DNA sequence analysis of rust fungi on garlic and chives from California, Phytopathology, 94, 569-577, doi:10.1094/PHYTO.2004.94.6.569, 2004. (Pubitemid 38681965)
6. Anikster, Y., Eilam, T., Bushnell, W. R., and Kosman, E.: Spore dimensions of Puccinia species of cereal hosts as determined by image analysis, Mycologia, 97, 474-484, doi:10.3852/mycologia.97.2.474, 2005. (Pubitemid 40938816)
7. Aylor, D. E.: A framework for examining interregional aerial transport of fungal spores, Agr. Forest Meteorol., 38, 263-288, doi:10.1016/0168-1923(86) 90017-1, 1986.
8. Aylor, D. E.: Spread of plant disease on a continental scale: role of aerial dispersal of pathogens, Ecology, 84, 1989-1997, doi:10.1890/01-0619, 2003.
9. Bauer, H., Schueller, E., Weinke, G., Berger, A., Hitzenberger, R., Marr, I. L., and Puxbaum, H.: Significant contributions of fungal spores to the organic carbon and to the aerosol mass balance of the urban atmospheric aerosol, Atmos. Environ., 42, 5542-5549, doi:10.1016/j.atmosenv.2008.03.019, 2008.
10. Bockus,W.W., Bowden, R. L., Hunger, R. M., Morrill,W. L., Murray, T. D., and Smiley, R.W. (Eds.): Compendium of Wheat Diseases and Pests, 3rd edn., APS Press, St. Paul, Minnesota, 2010.
11. Bourgeois, Q. and Bey, I.: Pollution transport efficiency toward the Arctic: sensitivity to aerosol scavenging and source regions, J. Geophys. Res.-Atmos., 116, D08213, doi:10.1029/2010JD015096, 2011.
12. Bowers, R. M., Lauber, C. L., Wiedinmyer, C., Hamady, M., Hallar, A. G., Fall, R., Knight, R., and Fierer, N.: Characterization of airborne microbial communities at a high-elevation site and their potential to act as atmospheric ice nuclei, Appl. Environ. Microb., 75, 5121-5130, doi:10.1128/aem.00447-09, 2009.
13. Bruckart, W. L., McClay, A. S., Hambleton, S., Tropiano, R., and Hill-Rackette, G.: First report of Puccinia lagenophorae on common groundsel (Senecio vulgaris) in Canada, Plant Dis., 91, 1058-1058, doi:10.1094/PDIS-91-8- 1058C, 2007.
14. Burrows, S. M., Butler, T., Jöckel, P., Tost, H., Kerkweg, A., Pöschl, U., and Lawrence, M. G.: Bacteria in the global atmosphere-Part 2: Modeling of emissions and transport between different ecosystems, Atmos. Chem. Phys., 9, 9281-9297, doi:10.5194/acp-9-9281-2009, 2009.
15. Burrows, S. M., Rayner, P. J., Butler, T., and Lawrence, M. G.: Estimating bacteria emissions from inversion of atmospheric transport: sensitivity to modelled particle characteristics, Atmos. Chem. Phys., 13, 5473-5488, doi:10.5194/acp-13-5473-2013, 2013.
16. Calderon, C., Lacey, J., Mccartney, H. A., and Rosas, I.: Seasonal and diurnal-variation of airborne basidiomycete spore concentrations in Mexico City, Grana, 34, 260-268, doi:10.1080/00173139509429055, 1995.
17. Chernoff, D. I. and Bertram, A. K.: Effects of sulfate coatings on the ice nucleation properties of a biological ice nucleus and several types of minerals, J. Geophys. Res.-Atmos., 115, D20205, doi:10.1029/2010jd014254, 2010.
18. Connolly, P. J., Möhler, O., Field, P. R., Saathoff, H., Burgess, R., Choularton, T., and Gallagher, M.: Studies of heterogeneous freezing by three different desert dust samples, Atmos. Chem. Phys., 9, 2805-2824, doi:10.5194/acp-9-2805-2009, 2009.
19. Crawford, C., Reponen, T., Lee, T., Iossifova, Y., Levin, L., Adhikari, A., and Grinshpun, S. A.: Temporal and spatial variation of indoor and outdoor airborne fungal spores, pollen, and (1! 3)-d-glucan, Aerobiologia, 25, 147-158, doi:10.1007/s10453-009-9120-z, 2009.
20. Creamean, J. M., Suski, K. J., Rosenfeld, D., Cazorla, A., De-Mott, P. J., Sullivan, R. C., White, A. B., Ralph, F. M., Minnis, P., Comstock, J. M., Tomlinson, J. M., and Prather, K. A.: Dust and biological aerosols from the Sahara and Asia influence precipitation in the western US, Science, 339, 1572-1578, doi:10.1126/science.1227279, 2013.
21. Cummins, G. B. and Husain, S. M.: The rust fungi on the genus Aristida, B. Torrey Bot. Club, 93, 56-67, 1966.
22. Delort, A.-M., Vaïtilingom, M., Amato, P., Sancelme, M., Parazols, M., Mailhot, G., Laj, P., and Deguillaume, L.: A short overview of the microbial population in clouds: potential roles in atmospheric chemistry and nucleation processes, Atmos. Res., 98, 249-260, doi:10.1016/j.atmosres.2010.07.004, 2010.
23. DeMott, P. J. and Prenni, A. J.: New directions: need for defining the numbers and sources of biological aerosols acting as ice nuclei, Atmos. Environ., 44, 1944-1945, doi:10.1016/j.atmosenv.2010.02.032, 2010.
24. Després, V. R., Huffman, J. A., Burrows, S. M., Hoose, C., Safatov, A. S., Buryak, G., Fröhlich-Nowoisky, J., Elbert, W., Andreae, M. O., Pöschl, U., and Jaenicke, R.: Primary biological aerosol particles in the atmosphere: a review, Tellus B, 64, 15598, doi:10.3402/tellusb.v64i0.15598, 2012.
25. Dymarska, M., Murray, B. J., Sun, L. M., Eastwood, M. L., Knopf, D. A., and Bertram, A. K.: Deposition ice nucleation on soot at temperatures relevant for the lower troposphere, J. Geophys. Res.-Atmos., 111, D04204, doi:10.1029/2005JD006627, 2006.
26. Ebner, M. R., Haselwandter, K., and Frank, A.: Seasonal fluctuations of airborne fungal allergens, Mycol. Res., 92, 170-176, 1989. (Pubitemid 20424561)
27. Elbert, W., Taylor, P. E., Andreae, M. O., and Pöschl, U.: Contribution of fungi to primary biogenic aerosols in the atmosphere: wet and dry discharged spores, carbohydrates, and inorganic ions, Atmos. Chem. Phys., 7, 4569-4588, doi:10.5194/acp-7-4569-2007, 2007. (Pubitemid 47385649)
28. Fröhlich-Nowoisky, J., Pickersgill, D. A., Després, V. R., and Pöschl, U.: High diversity of fungi in air particulate matter, P. Natl. Acad. Sci. USA, 106, 12814-12819, doi:10.1073/pnas.0811003106, 2009.
29. Fröhlich-Nowoisky, J., Burrows, S. M., Xie, Z., Engling, G., Solomon, P. A., Fraser, M. P., Mayol-Bracero, O. L., Artaxo, P., Begerow, D., Conrad, R., Andreae, M. O., Després, V. R., and Pöschl, U.: Biogeography in the air: fungal diversity over land and oceans, Biogeosciences, 9, 1125-1136, doi:10.5194/bg-9-1125-2012, 2012.
30. Fulton, J. D.: Microorganisms of upper atmosphere, III. Relationship between altitude and micropopulation, Appl. Microbiol., 14, 237-240, 1966.
31. Garcia, E., Hill, T. C. J., Prenni, A. J., DeMott, P. J., Franc, G. D., and Kreidenweis, S. M.: Biogenic ice nuclei in boundary layer air over two US High Plains agricultural regions, J. Geophys. Res.-Atmos., 117, D18209, doi:10.1029/2012JD018343, 2012.
32. Gilbertson, R. L. and Ryvarden, L.: North American Polypores, Fungiflora, Oslo, 1987.
33. Gläser, G., Kerkweg, A., and Wernli, H.: The mineral dust cycle in EMAC 2.40: sensitivity to the spectral resolution and the dust emission scheme, Atmos. Chem. Phys., 12, 1611-1627, doi:10.5194/acp-12-1611-2012, 2012.
34. Goncalves, F. L. T., Bauer, H., Cardoso, M. R. A., Pukinskas, S., Matos, D., Melhem, M., and Puxbaum, H.: Indoor and outdoor atmospheric fungal spores in the So Paulo metropolitan area (Brazil): species and numeric concentrations, Int. J. Biometeorol., 54, 347-355, 2010.
35. Gregory, P. H.: Spore content of the atmosphere near the ground, Nature, 170, 475-477, doi:10.1038/170475a0, 1952.
36. Gregory, P. H.: Distribution of airborne pollen and spores and their long-distance transport, Pure Appl. Geophys., 116, 309-315, doi:10.1007/ bf01636888, 1978.
37. Griffin, D. W.: Terrestrial microorganisms at an altitude of 20,000m in Earth's atmosphere, Aerobiologia, 20, 135-140, doi:10.1023/B:AERO.0000032948. 84077.12, 2004. (Pubitemid 38918905)
38. Hader, J. D., Wright, T. P., and Petters, M. D.: Contribution of pollen to atmospheric ice nuclei concentrations, Atmos. Chem. Phys., 14, 5433-5449, doi:10.5194/acp-14-5433-2014, 2014.
39. Haga, D. I., Iannone, R., Wheeler, M. J., Mason, R., Polishchuk, E. A., Fetch Jr., T., Van der Kamp, B. J., McKendry, I. G., and Bertram, A. K.: Ice nucleation properties of rust and bunt fungal spores and their transport to high altitudes where they can cause heterogeneous freezing, J. Geophys. Res.-Atmos., 118, 7260-7272, doi:10.1002/jgrd.50556, 2013.
40. Hasegawa, Y., Ishihara, Y., and Tokuyama, T.: Characteristics of ice-nucleation activity in Fusarium avenaceum IFO 7158, Biosci. Biotechnol. Biochem., 58, 2273-2274, 1994.
41. Hasnain, S. M., Fatima, K., Al-Frayh, A., and Al-Sedairy, S. T.: Prevalence of airborne basidiospores in three coastal cities of Saudi Arabia, Aerobiologia, 21, 139-145, 2005. (Pubitemid 41127059)
42. Heald, C. L. and Spracklen, D. V.: Atmospheric budget of primary biological aerosol particles from fungal spores, Geophys. Res. Lett., 36, L09806, doi:10.1029/2009GL037493, 2009.
43. Henning, S., Bojinski, S., Diehl, K., Ghan, S., Nyeki, S., Weingartner, E., Wurzler, S., and Baltensperger, U.: Aerosol partitioning in natural mixed-phase clouds, Geophys. Res. Lett., 31, L06101, doi:10.1029/2003GL019025, 2004.
44. Herrero, A. D., Ruiz, S. S., Bustillo, M. G., and Morales, P. C.: Study of airborne fungal spores in Madrid, Spain, Aerobiologia, 22, 135-142, doi:10.1007/s10453-006-9025-z, 2006. (Pubitemid 44367993)
45. Hibbett, D. S., Binder, M., Bischoff, J. F., Blackwell, M., Cannon, P. F., Eriksson, O. E., Huhndorf, S., James, T., Kirk, P. M., Lucking, R., Lumbsch, H. T., Lutzoni, F., Matheny, P. B., Mclaughlin, D. J., Powell, M. J., Redhead, S., Schoch, C. L., Spatafora, J. W., Stalpers, J. A., Vilgalys, R., Aime, M. C., Aptroot, A., Bauer, R., Begerow, D., Benny, G. L., Castlebury, L. A., Crous, P.W., Dai, Y. C., Gams,W., Geiser, D. M., Griffith, G.W., Gueidan, C., Hawksworth, D. L., Hestmark, G., Hosaka, K., Humber, R. A., Hyde, K. D., Ironside, J. E., Koljalg, U., Kurtzman, C. P., Larsson, K. H., Lichtwardt, R., Longcore, J., Miadlikowska, J., Miller, A., Moncalvo, J. M., Mozley-Standridge, S., Oberwinkler, F., Parmasto, E., Reeb, V., Rogers, J. D., Roux, C., Ryvarden, L., Sampaio, J. P., Schussler, A., Sugiyama, J., Thorn, R. G., Tibell, L., Untereiner,W. A.,Walker, C.,Wang, Z., Weir, A., Weiss, M., White, M. M., Winka, K., Yao, Y. J., and Zhang, N.: A higher-level phylogenetic classification of the Fungi, Mycol. Res., 111, 509-547, 2007. (Pubitemid 46915419)
46. Hirst, J. M.: Changes in atmospheric spore content: diurnal periodicity and the effects of weather, T. Brit. Mycol. Soc., 36, 375-393, 1953.
47. Hirst, J. M., Stedman, O. J., and Hogg, W. H.: Long-distance spore transport: methods of measurement, vertical spore profiles and the detection of immigrant spores, J. Gen. Microbiol., 48, 329-355, 1967.
48. Ho, H.-M., Rao, C. Y., Hsu, H.-H., Chiu, Y.-H., Liu, C.-M., and Chao, H. J.: Characteristics and determinants of ambient fungal spores in Hualien, Taiwan, Atmos. Environ., 32, 5839-5850, doi:10.1016/j.atmosenv.2005.06.034, 2005.
49. Hoose, C., Kristjansson, J. E., and Burrows, S. M.: How important is biological ice nucleation in clouds on a global scale?, Environ. Res. Lett., 5, 024009, doi:10.1088/1748-9326/5/2/024009, 2010a.
50. Hoose, C., Kristjánsson, J. E., Chen, J. P., and Hazra, A.: A classical-theory-based parameterization of heterogeneous ice nucleation by mineral dust, soot, and biological particles in a global climate model, J. Atmos. Sci., 67, 2483-2503, doi:10.1175/2010JAS3425.1, 2010b.
51. Hoose, C. and Möhler, O.: Heterogeneous ice nucleation on atmospheric aerosols: a review of results from laboratory experiments, Atmos. Chem. Phys., 12, 9817-9854, doi:10.5194/acp-12-9817-2012, 2012.
52. Horner, W. E., Helbling, A., Salvaggio, J. E., and Lehrer, S. B.: Fungal allergens, Clin. Microbiol. Rev., 8, 161-179, 1995.
53. Huffman, J. A., Prenni, A. J., DeMott, P. J., Pöhlker, C., Mason, R. H., Robinson, N. H., Fröhlich-Nowoisky, J., Tobo, Y., Després, V. R., Garcia, E., Gochis, D. J., Harris, E., Müller-Germann, I., Ruzene, C., Schmer, B., Sinha, B., Day, D. A., Andreae, M. O., Jimenez, J. L., Gallagher, M., Kreidenweis, S. M., Bertram, A. K., and Pöschl, U.: High concentrations of biological aerosol particles and ice nuclei during and after rain, Atmos. Chem. Phys., 13, 6151-6164, doi:10.5194/acp-13-6151-2013, 2013.
54. Iannone, R., Chernoff, D. I., Pringle, A., Martin, S. T., and Bertram, A. K.: The ice nucleation ability of one of the most abundant types of fungal spores found in the atmosphere, Atmos. Chem. Phys., 11, 1191-1201, doi:10.5194/acp-11-1191-2011, 2011.
55. Iglesias Fernández, I., Seijo Coello, M. C., Fernández González, M., and Escuredo Pérez, O.: Aerobiological monitoring of Aspergillus/Penicillium spores during the potato storage, Aerobiologia, 28, 213-219, doi:10.1007/s10453-011-9229-8, 2012.
56. Imshenetsky, A. A., Lysenko, S. V., and Kazakov, G. A.: Upper boundary of the biosphere, Appl. Environ. Microb., 35, 1-5, 1978. (Pubitemid 8275042)
57. Isard, S. A., Gage, S. H., Comtois, P., and Russo, J. M.: Principles of the atmospheric pathway for invasive species applied to soybean rust, Bioscience, 55, 851-861, doi:10.1641/0006-3568(2005)055[0851:potapf]2.0.co;2, 2005. (Pubitemid 41443699)
58. James, T. Y., Kauff, F., Schoch, C. L., Matheny, P. B., Hofstetter, V., Cox, C. J., Celio, G., Gueidan, C., Fraker, E., Miadlikowska, J., Lumbsch, H. T., Rauhut, A., Reeb, V., Arnold, A. E., Amtoft, A., Stajich, J. E., Hosaka, K., Sung, G. H., Johnson, D., O'Rourke, B., Crockett, M., Binder, M., Curtis, J. M., Slot, J. C., Wang, Z., Wilson, A. W., Schussler, A., Longcore, J. E., O'Donnell, K., Mozley-Standridge, S., Porter, D., Letcher, P. M., Powell, M. J., Taylor, J. W., White, M. M., Griffith, G. W., Davies, D. R., Humber, R. A., Morton, J. B., Sugiyama, J., Rossman, A. Y., Rogers, J. D., Pfister, D. H., Hewitt, D., Hansen, K., Hambleton, S., Shoemaker, R. A., Kohlmeyer, J., Volkmann-Kohlmeyer, B., Spotts, R. A., Serdani, M., Crous, P. W., Hughes, K. W., Matsuura, K., Langer, E., Langer, G., Untereiner, W. A., Lucking, R., Budel, B., Geiser, D. M., Aptroot, A., Diederich, P., Schmitt, I., Schultz, M., Yahr, R., Hibbett, D. S., Lutzoni, F., McLaughlin, D. J., Spatafora, J.W., and Vilgalys, R.: Reconstructing the early evolution of Fungi using a six-gene phylogeny, Nature, 443, 818-822, 2006. (Pubitemid 44622687)
59. Jayaweera, K. and Flanagan, P.: Investigations on biogenic ice nuclei in the Arctic atmosphere, Geophys. Res. Lett., 9, 94-97, doi:10.1029/ GL009i001p00094, 1982.
60. Jöckel, P., Sander, R., Kerkweg, A., Tost, H., and Lelieveld, J.: Technical note: The Modular Earth Submodel System (MESSy)-a new approach towards Earth System Modeling, Atmos. Chem. Phys., 5, 433-444, doi:10.5194/acp-5-433- 2005, 2005. (Pubitemid 40405294)
61. Jöckel, P., Tost, H., Pozzer, A., Brühl, C., Buchholz, J., Ganzeveld, L., Hoor, P., Kerkweg, A., Lawrence, M. G., Sander, R., Steil, B., Stiller, G., Tanarhte, M., Taraborrelli, D., van Aardenne, J., and Lelieveld, J.: The atmospheric chemistry general circulation model ECHAM5/MESSy1: consistent simulation of ozone from the surface to the mesosphere, Atmos. Chem. Phys., 6, 5067-5104, doi:10.5194/acp-6-5067-2006, 2006. (Pubitemid 44717487)
62. Jones, C. L., Lonergan, G. T., and Mainwaring, D. E.: The use of image analysis for spore counts of white-rot fungi, Biotechnol. Tech., 6, 417-422, 1992.
63. Kelly, C. D. and Pady, S. M.: Microbiological studies of air over some nonarctic regions of Canada, Can. J. Botany, 31, 90-106, 1953.
64. Kerkweg, A., Sander, R., Tost, H., and Jöckel, P.: Technical note: Implementation of prescribed (OFFLEM), calculated (ONLEM), and pseudo-emissions (TNUDGE) of chemical species in the Modular Earth Submodel System (MESSy), Atmos. Chem. Phys., 6, 3603-3609, doi:10.5194/acp-6-3603-2006, 2006. (Pubitemid 44329040)
65. Khattab, A. and Levetin, E.: Effect of sampling height on the concentration of airborne fungal spores, Ann. Allerg. Asthma Im., 101, 529-534, doi:10.1016/S1081-1206(10)60293-1, 2008.
66. Kim, K. S. and Beresford, R. M.: Use of a spectrum model and satellite cloud data in the simulation of wheat stripe rust (Puccinia striiformis) dispersal across the Tasman Sea in 1980, Agr. Forest Meteorol., 148, 1374-1382, doi:10.1016/j.agrformet.2008.04.004, 2008.
67. Koop, T., Ng, H. P., Molina, L. T., and Molina, M. J.: A new optical technique to study aerosol phase transitions: the nucleation of ice from H2SO4 aerosols, J. Phys. Chem. A, 102, 8924-8931, doi:10.1021/jp9828078, 1998. (Pubitemid 128576432)
68. Laundon, G. F. and Waterston, J. M.: Hemileia vastatrix-CMI descriptions of pathogenic fungi and bacteria, No. 1, Commonwealth Mycological Institute, Kew, UK, 1964.
69. Lawrence, M. G. and Rasch, P. J.: Tracer transport in deep convective updrafts: plume ensemble vs. bulk formulations, J. Atmos. Sci., 62, 2880-2894, doi:10.1175/JAS3505.1, 2005. (Pubitemid 41410839)
70. Lelieveld, J., Kunkel, D., and Lawrence, M. G.: Global risk of radioactive fallout after major nuclear reactor accidents, Atmos. Chem. Phys., 12, 4245-4258, doi:10.5194/acp-12-4245-2012, 2012.
71. Li, D. W.: Release and dispersal of basidiospores from Amanita muscaria varalba and their infiltration into a residence, Mycol. Res., 109, 1235-1242, doi:10.1017/S0953756205003953, 2005. (Pubitemid 41411821)
72. Li, D. W. and Kendrick, B.: A year-round outdoor aeromycological study in Waterloo, Ontario, Canada, Grana, 34, 199-207, 1995. (Pubitemid 26453355)
73. Lincoff, G. H.: The Audubon Society Field Guide to North American Mushrooms, Aldred A. Knopf Inc., New York, 1981.
74. Madelin, T. M.: Fungal aerosols: a review, J. Aerosol Sci., 25, 1405-1412, doi:10.1016/0021-8502(94)90216-x, 1994.
75. Magarey, R. D., Fowler, G. A., Borchert, D. M., Sutton, T. B., Colunga-Garcia, M., and Simpson, J. A.: NAPPFAST: an internet system for the weather-based mapping of plant pathogens, Plant Dis., 91, 336-345, doi:10.1094/pdis-91-4-0336, 2007. (Pubitemid 46466683)
76. Magyar, D., Frenguelli, G., Bricchi, E., Tedeschini, E., Csontos, P., Li, D. W., and Bobvos, J.: The biodiversity of air spora in an Italian vineyard, Aerobiologia, 25, 99-109, doi:10.1007/s10453-009-9115-9, 2009.
77. Mallo, A. C., Nitiu, D. S., and Gardella Sambeth, M. C.: Airborne fungal spore content in the atmosphere of the city of La Plata, Argentina, Aerobiologia, 27, 77-84, doi:10.1007/s10453-010-9172-0, 2011.
78. Mathre, D. E. (Ed.): Compendium of Barley Diseases, APS Press, St. Paul, 1982.
79. Mitakakis, T. Z. and Guest, D. I.: A fungal spore calendar for the atmosphere of Melbourne, Australia, for the year 1993, Aerobiologia, 17, 171-176, doi:10.1023/A:1011028412526, 2001. (Pubitemid 32538447)
80. Mitchell, A. D. and Walter, M.: Species of Agaricus occurring in New Zealand, New Zeal. J. Bot., 37, 715-725, 1999. (Pubitemid 30086340)
81. Möhler, O., DeMott, P. J., Vali, G., and Levin, Z.: Microbiology and atmospheric processes: the role of biological particles in cloud physics, Biogeosciences, 4, 1059-1071, doi:10.5194/bg-4-1059-2007, 2007. (Pubitemid 350211419)
82. Morales, J., Gonzalez-Minero, F. J., Carrasco, M., Ogalla, V. M., and Candau, P.: Airborne basidiospores in the atmosphere of Seville (South Spain), Aerobiologia, 22, 127-134, 2006. (Pubitemid 44367992)
83. Morris, C. E., Georgakopoulos, D. G., and Sands, D. C.: Ice nucleation active bacteria and their potential role in precipitation, J. Phys. IV, 121, 87-103, doi:10.1051/jp4:2004121004, 2004.
84. Morris, C. E., Sands, D. C., Bardin, M., Jaenicke, R., Vogel, B., Leyronas, C., Ariya, P. A., and Psenner, R.: Microbiology and atmospheric processes: research challenges concerning the impact of airborne micro-organisms on the atmosphere and climate, Biogeosciences, 8, 17-25, doi:10.5194/bg-8-17- 2011, 2011.
85. Morris, C. E., Conen, F., Huffman, J. A., Phillips, V., Pöschl, U., and Sands, D. C.: Bioprecipitation: a feedback cycle linking Earth history, ecosystem dynamics and land use through biological ice nucleators in the atmosphere, Glob. Change Biol., 20, 341-351, doi:10.1111/gcb.12447, 2013a.
86. Morris, C. E., Sands, D. C., Glaux, C., Samsatly, J., Asaad, S., Moukahel, A. R., Gonçalves, F. L. T., and Bigg, E. K.: Urediospores of rust fungi are ice nucleation active at ?10-C and harbor ice nucleation active bacteria, Atmos. Chem. Phys., 13, 4223-4233, doi:10.5194/acp-13-4223-2013, 2013b.
87. Murray, B. J., O'Sullivan, D., Atkinson, J. D., andWebb, M. E.: Ice nucleation by particles immersed in supercooled cloud droplets, Chem. Soc. Rev., 41, 6519-6554, doi:10.1039/c2cs35200a, 2012.
88. Nayar, T. S. and Jothish, P. S.: An assessment of the air quality in indoor and outdoor air with reference to fungal spores and pollen grains in four working environments in Kerala, India, Aerobiologia, 29, 131-152, doi:10.1007/s10453-012-9269-8, 2013.
89. Niemand, M., Möhler, O., Vogel, B., Vogel, H., Hoose, C., Connolly, P., Klein, H., Bingemer, H., DeMott, P. J., Skrotzki, J., and Leisner, T.: A particle-surface-area-based parameterization of immersion freezing on desert dust particles, J. Atmos. Sci., 69, 3077-3092, doi:10.1175/JAS-D-11-0249.1, 2012.
90. Oliveira, M., Ribeiro, H., and Abreu, I.: Annual variation of fungal spores in atmosphere of Porto: 2003, Ann. Agr. Env. Med., 12, 309-315, 2005.
91. Oliveira, M., Ribeiro, H., Delgado, J. L., and Abreu, I.: Seasonal and intradiurnal variation of allergenic fungal spores in urban and rural areas of the North of Portugal, Aerobiologia, 25, 85-98, 2009a.
92. Oliveira, M., Ribeiro, H., Delgado, J. L., and Abreu, I.: The effects of meteorological factors on airborne fungal spore concentration in two areas differing in urbanisation level, Int. J. Biometeorol., 53, 61-73, doi:10.1007/s00484-008-0191-2, 2009b. (Pubitemid 50349119)
93. Pady, S. M. and Kapica, L.: Fungi in air over the Atlantic Ocean, Mycologia, 47, 34-50, doi:10.2307/3755754, 1955.
94. Pady, S. M. and Kelly, C. D.: Numbers of fungi and bacteria in transatlantic air, Science, 117, 607-609, doi:10.1126/science.117.3048.607, 1953.
95. Pady, S. M. and Kelly, C. D.: Aerobiological studies of fungi and bacteria over the Atlantic Ocean, Can. J. Bot., 32, 202-212, 1954.
96. Pan, Z., Yang, X. B., Pivonia, S., Xue, L., Pasken, R., and Roads, J.: Long-term prediction of soybean rust entry into the Continental United States, Plant Dis., 90, 840-846, doi:10.1094/PD-90-0840, 2006.
97. Pasanen, A. L., Pasanen, P., Jantunen, M. J., and Kalliokoski, P.: Significance of air humidity and air velocity for fungal spore release into the air, Atmos. Environ., 25, 459-462, 1991.
98. Pfender, W., Graw, R., Bradley, W., Carney, M., and Maxwell, L.: Use of a complex air pollution model to estimate dispersal and deposition of grass stem rust urediniospores at landscape scale, Agr. Forest Meteorol., 139, 138-153, doi:10.1016/j.agrformet.2006.06.007, 2006. (Pubitemid 44442502)
99. Phillips, V. T. J., Andronache, C., Christner, B., Morris, C. E., Sands, D. C., Bansemer, A., Lauer, A., McNaughton, C., and Seman, C.: Potential impacts from biological aerosols on ensembles of continental clouds simulated numerically, Biogeosciences, 6, 987-1014, doi:10.5194/bg-6-987-2009, 2009.
100. Pöschl, U., Martin, S. T., Sinha, B., Chen, Q., Gunthe, S. S., Huffman, J. A., Borrmann, S., Farmer, D. K., Garland, R. M., Helas, G., Jimenez, J. L., King, S. M., Manzi, A., Mikhailov, E., Pauliquevis, T., Petters, M. D., Prenni, A. J., Roldin, P., Rose, D., Schneider, J., Su, H., Zorn, S. R., Artaxo, P., and Andreae, M. O.: Rainforest aerosols as biogenic nuclei of clouds and precipitation in the Amazon, Science, 329, 1513-1516, doi:10.1126/science. 1191056, 2010.
101. Pouleur, S., Richard, C., Martin, J. G., and Antoun, H.: Ice nucleation activity in Fusarium acuminatum and Fusarium avenaceum, Appl. Environ. Microbiol., 58, 2960-2964, 1992.
102. Pratt, K. A., DeMott, P. J., French, J. R., Wang, Z., Westphal, D. L., Heymsfield, A. J., Twohy, C. H., Prenni, A. J., and Prather, K. A.: In situ detection of biological particles in cloud ice-crystals, Nat. Geosci., 2, 397-400, doi:10.1038/ngeo521, 2009.
103. Prenni, A. J., Demott, P. J., Rogers, D. C., Kreidenweis, S. M., McFarquhar, G. M., Zhang, G., and Poellot, M. R.: Ice nuclei characteristics from M-PACE and their relation to ice formation in clouds, Tellus B, 61, 436-448, doi:10.1111/j.1600-0889.2009.00415.x, 2009.
104. Proctor, B. E. and Parker, B. W.: Microbiology of the upper air, III. An improved apparatus and technique for upper air investigations, J. Bacteriol., 36, 175-185, 1938.
105. Pummer, B. G., Atanasova, L., Bauer, H., Bernardi, J., Druzhinina, I. S., and Grothe, H.: Spores of most common airborne fungi reveal no ice nucleation activity, Biogeosciences Discuss., 10, 10125-10141, doi:10.5194/bgd-10-10125- 2013, 2013.
106. Pyrri, I. and Kapsanaki-Gotsi, E.: A comparative study on the airborne fungi in Athens, Greece, by viable and non-viable sampling methods, Aerobiologia, 23, 3-15, doi:10.1007/s10453-006-9039-6, 2007. (Pubitemid 46723601)
107. Pyrri, I. and Kapsanaki-Gotsi, E.: Diversity and annual fluctuations of culturable airborne fungi in Athens, Greece: a 4-year study, Aerobiologia, 28, 249-262, doi:10.1007/s10453-011-9233-z, 2012.
108. Quintero, E., Rivera-Mariani, F., and 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, 26, 113-124, doi:10.1007/s10453-009-9148-0, 2010.
109. Raper, K. B., Thom, C., and Fennel, D. I.: A Manual of the Penicillia, The Williams & Williams Company, Baltimore, 1949.
110. Roeckner, E., Bäuml, G., Bonaventura, L., Brokopf, R., Esch, M., Giorgetta, M., Hagemann, S., Kirchner, I., Kornblueh, L., Manzini, E., Rhodin, A., Schlese, U., Schulzweida, U., and Tompkins, A.: The Atmospheric General Circulation Model ECHAM5, Part 1: Model Description, Max Planck Institute for Meteorology, Hamburg, 349 pp., 2003.
111. Sabariego, S., de la Guardia, C. D., and Alba, F.: The effect of meteorological factors on the daily variation of airborne fungal spores in Granada (southern Spain), Int. J. Biometeorol., 44, 1-5, doi:10.1007/ s004840050131, 2000.
112. Sands, D. C., Langhans, V. E., Scharen, A. L., and de Smet, G.: The association between bacteria and rain and possible meteorological implications, J. Hungarian Meteorol. Serv., 86, 148-152, 1982.
113. Schubert, K., Groenewald, J. Z., Braun, U., Dijksterhuis, J., Starink, M., Hill, C. F., Zalar, P., de Hoog, G. S., and Crous, P.W.: Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics, Stud. Mycol., 58, 105-156, doi:10.3114/sim.2007.58.05, 2007. (Pubitemid 47572402)
114. Sesartic, A., Lohmann, U., and Storelvmo, T.: Bacteria in the ECHAM5-HAM global climate model, Atmos. Chem. Phys., 12, 8645-8661, doi:10.5194/acp-12- 8645-2012, 2012.
115. Sesartic, A., Lohmann, U., and Storelvmo, T.: Modelling the impact of fungal spore ice nuclei on clouds and precipitation, Environ. Res. Lett., 8, 014029, doi:10.1088/1748-9326/8/1/014029, 2013.
116. Shelton, B. G., Kirkland, K. H., Flanders,W. D., and Morris, G. K.: Profiles of airborne fungi in buildings and outdoor environments in the United States, Appl. Environ. Microb., 68, 1743-1753, 2002. (Pubitemid 34279981)
117. Skelsey, P., Holtslag, A. A. M., and van der Werf,W.: Development and validation of a quasi-Gaussian plume model for the transport of botanical spores, Agr. Forest Meteorol., 148, 1383-1394, doi:10.1016/j.agrformet.2008.04. 006, 2008.
118. Smith, D. J., Griffin, D. W., and Schuerger, A. C.: Stratospheric microbiology at 20 km over the Pacific Ocean, Aerobiologia, 26, 35-46, doi:10.1007/s10453-009-9141-7, 2010.
119. Spracklen, D. V. and Heald, C. L.: The contribution of fungal spores and bacteria to regional and global aerosol number and ice nucleation immersion freezing rates, Atmos. Chem. Phys. Discuss., 13, 32459-32481, doi:10.5194/acpd-13-32459-2013, 2013.
120. Tobo, Y., Prenni, A. J., DeMott, P. J., Huffman, J. A., Mc-Cluskey, C. S., Tian, G., Pöhlker, C., Pöschl, U., and Kreidenweis, S. M.: Biological aerosol particles as a key determinant of ice nuclei populations in a forest ecosystem, J. Geophys. Res.-Atmos., 118, 10100-10110, doi:10.1002/jgrd.50801, 2013.
121. Tost, H., Jöckel, P., Kerkweg, A., Sander, R., and Lelieveld, J.: Technical note: A new comprehensive SCAVenging submodel for global atmospheric chemistry modelling, Atmos. Chem. Phys., 6, 565-574, doi:10.5194/acp-6-565-2006, 2006.
122. Tost, H., Lawrence, M. G., Brühl, C., Jöckel, P., The GABRIEL Team, and The SCOUT-O3-DARWIN/ACTIVE Team: uncertainties in atmospheric chemistry modelling due to convection parameterisations and subsequent scavenging, Atmos. Chem. Phys., 10, 1931-1951, doi:10.5194/acp-10-1931-2010, 2010.
123. Troutt, C. and Levetin, E.: Correlation of spring spore concentrations and meteorological conditions in Tulsa, Oklahoma, Int. J. Biometeorol., 45, 64-74, doi:10.1007/s004840100087, 2001. (Pubitemid 33626743)
124. Vali, G.: Quantitative evaluation of experimental results on heterogeneous freezing nucleation of supercooled liquids, J. Atmos. Sci., 28, 402-409, doi:10.1175/1520-0469(1971)0282.0.CO;2, 1971.
125. Vanky, K.: Illustrated Genera of Smut Fungi, Gustav Fischer Verlag GmbH, Stuttgart, 1987..
126. Verheggen, B., Cozic, J., Weingartner, E., Bower, K., Mertes, S., Connolly, P., Gallagher, M., Flynn, M., Choularton, T., and Baltensperger, U.: Aerosol partitioning between the interstitial and the condensed phase in mixed-phase clouds, J. Geophys. Res.-Atmos., 112, D23202, doi:10.1029/ 2007JD008714, 2007.
127. Wang, H., Yang, X. B., and Ma, Z.: Long-distance spore transport of wheat stripe rust pathogen from Sichuan, Yunnan, and Guizhou in southwestern China, Plant Dis., 94, 873-880, doi:10.1094/pdis-94-7-0873, 2010.
128. Webster, J. and Weber, R.: Introduction to Fungi, Cambridge University Press, Cambridge, UK, 2007.
129. Wheeler, M. J. and Bertram, A. K.: Deposition nucleation on mineral dust particles: a case against classical nucleation theory with the assumption of a single contact angle, Atmos. Chem. Phys., 12, 1189-1201, doi:10.5194/acp-12- 1189-2012, 2012.
130. Wilkinson, D. M., Koumoutsaris, S., Mitchell, E. A. D., and Bey, I.: Modelling the effect of size on the aerial dispersal of microorganisms, J. Biogeogr., 39, 89-97, doi:10.1111/j.1365-2699.2011.02569.x, 2012.
131. Wu, P. C., Tsai, J. C., Li, F. C., Lung, S. C., and Su, H. J.: Increased levels of ambient fungal spores in Taiwan are associated with dust events from China, Atmos. Environ., 38, 4879-4886, doi:10.1016/j.atmosenv.2004.05.039, 2004. (Pubitemid 39078328)
132. Yamamoto, N., Bibby, K., Qian, J., Hospodsky, D., Rismani-Yazdi, H., Nazaroff, W. W., and Peccia, J.: Particle-size distributions and seasonal diversity of allergenic and pathogenic fungi in outdoor air, ISME J., 6, 1801-1811, doi:10.1038/ismej.2012.30, 2012.
133. Zhang, K., O'Donnell, D., Kazil, J., Stier, P., Kinne, S., Lohmann, U., Ferrachat, S., Croft, B., Quaas, J., Wan, H., Rast, S., and Feichter, J.: The global aerosol-climate model ECHAM-HAM, version 2: sensitivity to improvements in process representations, Atmos. Chem. Phys., 12, 8911-8949, doi:10.5194/acp-12-8911-2012, 2012.