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Long-Distance Dispersal of Fungi

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  • Authors: Jacob J. Golan1, Anne Pringle2
  • Editors: Joseph Heitman3, Pedro W. Crous4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Botany, Department of Bacteriology, University of Wisconsin–Madison, Madison, WI 35706; 2: Department of Botany, Department of Bacteriology, University of Wisconsin–Madison, Madison, WI 35706; 3: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 4: CBS-KNAW Fungal Diversity Centre, Royal Dutch Academy of Arts and Sciences, Utrecht, The Netherlands
  • Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0047-2016
  • Received 05 February 2017 Accepted 01 May 2017 Published 14 July 2017
  • Jacob J. Golan, jacobjgolan@gmail.com
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  • Abstract:

    Dispersal is a fundamental biological process, operating at multiple temporal and spatial scales. Despite an increasing understanding of fungal biodiversity, most research on fungal dispersal focuses on only a small fraction of species. Thus, any discussion of the dispersal dynamics of fungi as a whole is problematic. While abundant morphological and biogeographic data are available for hundreds of species, researchers have yet to integrate this information into a unifying paradigm of fungal dispersal, especially in the context of long-distance dispersal (LDD). Fungal LDD is mediated by multiple vectors, including meteorological phenomena (e.g., wind and precipitation), plants (e.g., seeds and senesced leaves), animals (e.g., fur, feathers, and gut microbiomes), and in many cases humans. In addition, fungal LDD is shaped by both physical constraints on travel and the ability of spores to survive harsh environments. Finally, fungal LDD is commonly measured in different ways, including by direct capture of spores, genetic comparisons of disconnected populations, and statistical modeling and simulations of dispersal data. To unify perspectives on fungal LDD, we propose a synthetic three-part definition that includes (i) an identification of the source population and a measure of the concentration of source inoculum and (ii) a measured and/or modeled dispersal kernel. With this information, LDD is defined as (iii) the distance found within the dispersal kernel beyond which only 1% of spores travel.

  • Citation: Golan J, Pringle A. 2017. Long-Distance Dispersal of Fungi. Microbiol Spectrum 5(4):FUNK-0047-2016. doi:10.1128/microbiolspec.FUNK-0047-2016.

Key Concept Ranking

Fungal Proteins
0.5926611
Asexual Spores
0.5899096
Sexual Spores
0.56417763
Fusarium graminearum
0.53125
0.5926611

References

1. Nathan R. 2001. The challenges of studying dispersal. Trends Ecol Evol 16:481–483 http://dx.doi.org/10.1016/S0169-5347(01)02272-8.
2. Finlay BJ. 2002. Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063 http://dx.doi.org/10.1126/science.1070710.
3. Hedlund B, Staley J. 2004. Microbial endemism and biogeography, p 225–231. In Bull AT (ed), Microbial Diversity and Bioprospecting. ASM Press, Washington, DC.
4. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreås L, Reysenbach AL, Smith VH, Staley JT. 2006. Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112 http://dx.doi.org/10.1038/nrmicro1341.
5. Crum H. 1972. The geographic origins of the mosses of North America & eastern deciduous forest. J Hattori Bot Lab 35:269–298.
6. Frahm JP. 2008. Diversity, dispersal and biogeography of bryophytes mosses. Biodivers Conserv 17:277–284 http://dx.doi.org/10.1007/s10531-007-9251-x.
7. McDaniel SF, Shaw AJ. 2003. Phylogeographic structure and cryptic speciation in the trans-Antarctic moss Pyrrhobryum mnioides. Evolution 57:205–215 http://dx.doi.org/10.1111/j.0014-3820.2003.tb00256.x.
8. Piñeiro R, Popp M, Hassel K, Listl D, Westergaard KB, Flatberg KI, Stenøien HK, Brochmann C. 2012. Circumarctic dispersal and long-distance colonization of South America: the moss genus Cinclidium. J Biogeogr 39:2041–2051 http://dx.doi.org/10.1111/j.1365-2699.2012.02765.x.
9. Szövényi P, Sundberg S, Shaw AJ. 2012. Long-distance dispersal and genetic structure of natural populations: an assessment of the inverse isolation hypothesis in peat mosses. Mol Ecol 21:5461–5472 http://dx.doi.org/10.1111/mec.12055.
10. Wolf PG, Schneider H, Ranker TA. 2001. Geographic distributions of homosporous ferns: does dispersal obscure evidence of vicariance? J Biogeogr 28:263–270 http://dx.doi.org/10.1046/j.1365-2699.2001.00531.x.
11. Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R. 2004. Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am J Bot 91:1582–1598 http://dx.doi.org/10.3732/ajb.91.10.1582.
12. Perrie L, Brownsey P. 2007. Molecular evidence for long-distance dispersal in the New Zealand pteridophyte flora. J Biogeogr 34:2028–2038 http://dx.doi.org/10.1111/j.1365-2699.2007.01748.x.
13. Schuettpelz E, Pryer KM. 2009. Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proc Natl Acad Sci USA 106:11200–11205 http://dx.doi.org/10.1073/pnas.0811136106. [PubMed]
14. Gage SH, Isard SA, Colunga-G M. 1999. Ecological scaling of aerobiological dispersal processes. Agric Meteorol 97:249–261 http://dx.doi.org/10.1016/S0168-1923(99)00070-2.
15. Staley JT, Gosink JJ. 1999. Poles apart: biodiversity and biogeography of sea ice bacteria. Annu Rev Microbiol 53:189–215 http://dx.doi.org/10.1146/annurev.micro.53.1.189.
16. Jones AM, Harrison RM. 2004. The effects of meteorological factors on atmospheric bioaerosol concentrations: a review. Sci Total Environ 326:151–180 http://dx.doi.org/10.1016/j.scitotenv.2003.11.021.
17. Vos M, Velicer GJ. 2008. Isolation by distance in the spore-forming soil bacterium Myxococcus xanthus. Curr Biol 18:386–391. [PubMed]
18. Smith DJ, Griffin DW, McPeters RD, Ward PD, Schuerger AC. 2011. Microbial survival in the stratosphere and implications for global dispersal. Aerobiologia 27:319–332 http://dx.doi.org/10.1007/s10453-011-9203-5.
19. Barberán A, Ladau J, Leff JW, Pollard KS, Menninger HL, Dunn RR, Fierer N. 2015. Continental-scale distributions of dust-associated bacteria and fungi. Proc Natl Acad Sci USA 112:5756–5761 http://dx.doi.org/10.1073/pnas.1420815112.
20. Brown JKM, Hovmøller MS. 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537–541 http://dx.doi.org/10.1126/science.1072678.
21. Bonito GM, Gryganskyi AP, Trappe JM, Vilgalys R. 2010. A global meta-analysis of Tuber ITS rDNA sequences: species diversity, host associations and long-distance dispersal. Mol Ecol 19:4994–5008 http://dx.doi.org/10.1111/j.1365-294X.2010.04855.x.
22. Talbot JM, Bruns TD, Taylor JW, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Liao H-L, Smith ME, Peay KG. 2014. Endemism and functional convergence across the North American soil mycobiome. Proc Natl Acad Sci USA 111:6341–6346 http://dx.doi.org/10.1073/pnas.1402584111.
23. Grantham NS, Reich BJ, Pacifici K, Laber EB, Menninger HL, Henley JB, Barberán A, Leff JW, Fierer N, Dunn RR. 2015. Fungi identify the geographic origin of dust samples. PLoS One 10:e0122605 http://dx.doi.org/10.1371/journal.pone.0122605.
24. Shigesada N, Kawasaki K. 1997. Biological Invasions: Theory and Practice. Oxford University Press, Oxford, United Kingdom.
25. Cain ML, Milligan BG, Strand AE. 2000. Long-distance seed dispersal in plant populations. Am J Bot 87:1217–1227 http://dx.doi.org/10.2307/2656714.
26. Clark JS. 1998. Why trees migrate so fast: confronting theory with dispersal biology and the paleorecord. Am Nat 152:204–224 http://dx.doi.org/10.1086/286162.
27. Nathan R, Muller-Landau HC. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285 http://dx.doi.org/10.1016/S0169-5347(00)01874-7.
28. Nathan R. 2006. Long-distance dispersal of plants. Science 313:786–788 http://dx.doi.org/10.1126/science.1124975.
29. Hawksworth D. 2001. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105:1422–1432 http://dx.doi.org/10.1017/S0953756201004725.
30. Peay KG, Garbelotto M, Bruns TD. 2010. Evidence of dispersal limitation in soil microorganisms: isolation reduces species richness on mycorrhizal tree islands. Ecology 91:3631–3640 http://dx.doi.org/10.1890/09-2237.1.
31. Hassett MO, Fischer MWF, Sugawara ZT, Stolze-Rybczynski J, Money NP. 2013. Splash and grab: biomechanics of peridiole ejection and function of the funicular cord in bird’s nest fungi. Fungal Biol 117:708–714 http://dx.doi.org/10.1016/j.funbio.2013.07.008.
32. Pringle A, Baker DM, Platt JL, Wares JP, Latgé JP, Taylor JW. 2005. Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59:1886–1899 http://dx.doi.org/10.1111/j.0014-3820.2005.tb01059.x.
33. Taylor JW, Turner E, Townsend JP, Dettman JR, Jacobson D. 2006. Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi. Philos Trans R Soc Lond B Biol Sci 361:1947–1963 http://dx.doi.org/10.1098/rstb.2006.1923.
34. Geml J, Tulloss RE, Laursen GA, Sazanova NA, Taylor DL. 2008. Evidence for strong inter- and intracontinental phylogeographic structure in Amanita muscaria, a wind-dispersed ectomycorrhizal basidiomycete. Mol Phylogenet Evol 48:694–701 http://dx.doi.org/10.1016/j.ympev.2008.04.029.
35. Ingold CT. 1965. Spore Liberation. Clarendon Press, Oxford, United Kingdom. [PubMed]
36. Li D-W. 2005. Release and dispersal of basidiospores from Amanita muscaria var. alba and their infiltration into a residence. Mycol Res 109:1235–1242 http://dx.doi.org/10.1017/S0953756205003953.
37. Whittier P, Wagner WH. 1971. The variation in spore size and germination in Dryopteris taxa. Am Fern J 61:123–127 http://dx.doi.org/10.2307/1546642.
38. Brown HM, Irving KR. 1973. The size and weight of common allergenic pollens. An investigation of their number per microgram and size distribution. Acta Allergol 28:132–137 http://dx.doi.org/10.1111/j.1398-9995.1973.tb01319.x.
39. Sundberg S. 2010. Size matters for violent discharge height and settling speed of Sphagnum spores: important attributes for dispersal potential. Ann Bot 105:291–300 http://dx.doi.org/10.1093/aob/mcp288.
40. Pringle A. 2013. Asthma and the diversity of fungal spores in air. PLoS Pathog 9:e1003371 http://dx.doi.org/10.1371/journal.ppat.1003371.
41. Parnell M, Burt PJA, Wilson K. 1998. The influence of exposure to ultraviolet radiation in simulated sunlight on ascospores causing black sigatoka disease of banana and plantain. Int J Biometeorol 42:22–27 http://dx.doi.org/10.1007/s004840050079.
42. Shinn EA, Smith GW, Prospero JM, Betzer P, Hayes ML, Garrison V, Barber RT. 2000. African dust and the demise of Caribbean coral reefs. Geophys Res Lett 27:3029–3032 http://dx.doi.org/10.1029/2000GL011599.
43. Griffin DW, Kellogg CA, Shinn EA. 2001. Dust in the wind: long range transport of dust in the atmosphere and its implications for global public and ecosystem health. Glob Change Hum Health 2:20–33 http://dx.doi.org/10.1023/A:1011910224374.
44. Kellogg CA, Griffin DW. 2006. Aerobiology and the global transport of desert dust. Trends Ecol Evol 21:638–644 http://dx.doi.org/10.1016/j.tree.2006.07.004.
45. Schmale DG III, Ross SD. 2015. Highways in the sky: scales of atmospheric transport of plant pathogens. Annu Rev Phytopathol 53:591–611 http://dx.doi.org/10.1146/annurev-phyto-080614-115942. [PubMed]
46. Barrett D. 2007. Maximizing the nutritional value of fruits & vegetables. Food Technol 61:40–44.
47. Ingold CT. 1953. Dispersal in Fungi. Clarendon Press, Oxford, United Kingdom.
48. Bullock J, Kenward R, Hails R. 2002. Dispersal Ecology. 42nd Symposium of the British Ecological Society, University of Reading, 2001. Blackwell Science, Malden, MA.
49. Clobert J, Baguette M, Benton TG, Bullock JM (ed). 2012. Dispersal Ecology and Evolution. Oxford University Press, Oxford, United Kingdom. http://dx.doi.org/10.1093/acprof:oso/9780199608898.001.0001
50. Holmer L, Stenlid J. 1993. The importance of inoculum size for the competitive ability of wood decomposing fungi. FEMS Microbiol Ecol 12:169–176 http://dx.doi.org/10.1111/j.1574-6941.1993.tb00029.x.
51. Prussin AJ, Marr LC, Schmale DG III, Stoll R, Ross SD. 2015. Experimental validation of a long-distance transport model for plant pathogens: application to Fusarium graminearum. Agric For Meteorol 460:1117–1121.
52. Rieux A, Soubeyrand S, Bonnot F, Klein EK, Ngando JE, Mehl A, Ravigne V, Carlier J, de Lapeyre de Bellaire L. 2014. Long-distance wind-dispersal of spores in a fungal plant pathogen: estimation of anisotropic dispersal kernels from an extensive field experiment. PLoS One 9:e103225 http://dx.doi.org/10.1371/journal.pone.0103225.
53. Aylor DE. 1986. A framework for examining inter-regional aerial transport of fungal spores. Agric Meteorol 38:263–288 http://dx.doi.org/10.1016/0168-1923(86)90017-1.
54. Nathan R, Klein E, Robledo-Arnuncio J, Revilla E. 2012. Dispersal kernels: review, p 187–210. In Clobert J, Baguette M, Benton TG, Bullock JM (ed), Dispersal Ecology and Evolution. Oxford University Press, Oxford, United Kingdom. http://dx.doi.org/10.1093/acprof:oso/9780199608898.003.0015
55. Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S, Njau P, Herrera-Foessel S, Singh PK, Singh S, Govindan V. 2011. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu Rev Phytopathol 49:465–481 http://dx.doi.org/10.1146/annurev-phyto-072910-095423.
56. Dam N. 2013. Spores do travel. Mycologia 105:1618–1622 http://dx.doi.org/10.3852/13-035.
57. Aylor DE, Taylor GS, Raynor GS. 1982. Long-range transport of tobacco blue mold spores. Agric Meteorol 27:217–232 http://dx.doi.org/10.1016/0002-1571(82)90007-3.
58. Aylor DE. 2003. Spread of plant disease on a continental scale: role of aerial dispersal of pathogens. Ecology 84:1989–1997 http://dx.doi.org/10.1890/01-0619.
59. Prussin AJ II, Li Q, Malla R, Ross SD, Schmale DG III. 2013. Monitoring the long-distance transport of Fusarium graminearum from field-scale sources of inoculum. Plant Dis 98:504–511 http://dx.doi.org/10.1094/PDIS-06-13-0664-RE.
60. Rivas G-G, Zapater M-F, Abadie C, Carlier J. 2004. Founder effects and stochastic dispersal at the continental scale of the fungal pathogen of bananas Mycosphaerella fijiensis. Mol Ecol 13:471–482 http://dx.doi.org/10.1046/j.1365-294X.2003.02043.x.
61. Geml J, Timling I, Robinson CH, Lennon N, Nusbaum HC, Brochmann C, Noordeloos ME, Taylor DL. 2012. An arctic community of symbiotic fungi assembled by long-distance dispersers: phylogenetic diversity of ectomycorrhizal basidiomycetes in Svalbard based on soil and sporocarp DNA. J Biogeogr 39:74–88 http://dx.doi.org/10.1111/j.1365-2699.2011.02588.x.
62. Matheny PB, Aime MC, Bougher NL, Buyck B, Desjardin DE, Horak E, Kropp BR, Lodge DJ, Soytong K, Trappe JM, Hibbett DS. 2009. Out of the palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae. J Biogeogr 36:577–592 http://dx.doi.org/10.1111/j.1365-2699.2008.02055.x.
63. Peterson KR, Pfister DH, Bell CD. 2010. Cophylogeny and biogeography of the fungal parasite Cyttaria and its host Nothofagus, southern beech. Mycologia 102:1417–1425 http://dx.doi.org/10.3852/10-048.
64. Zhan J, Pettway RE, McDonald BA. 2003. The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal Genet Biol 38:286–297 http://dx.doi.org/10.1016/S1087-1845(02)00538-8.
65. Linde CC, Zhan J, McDonald BA. 2002. Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology 92:946–955 http://dx.doi.org/10.1094/PHYTO.2002.92.9.946.
66. Prospero JM. 1999. Long-term measurements of the transport of African mineral dust to the southeastern United States: implications for regional air quality. J Geophys Res 104(D13):15917–15927 http://dx.doi.org/10.1029/1999JD900072.
67. Moulin C, Lambert CE, Dulac F, Dayan U. 1997. Control of atmospheric export of dust from North Africa by the North Atlantic oscillation. Nature 387:691–694 http://dx.doi.org/10.1038/42679.
68. Weir-Brush JR, Garrison VH, Smith GW, Shinn EA. 2004. The relationship between gorgonian coral Cnidaria: Gorgonacea diseases and African dust storms. Aerobiologia 20:119–126 http://dx.doi.org/10.1023/B:AERO.0000032949.14023.3a.
69. Hirst JM, Stedman OJ, Hurst GW. 1967. Long-distance spore transport: vertical sections of spore clouds over the sea. J Gen Microbiol 48:357–377 http://dx.doi.org/10.1099/00221287-48-3-357.
70. Maldonado-Ramirez SL, Schmale DG III, Shields EJ, Bergstrom GC. 2005. The relative abundance of viable spores of Gibberella zeae in the planetary boundary layer suggests the role of long-distance transport in regional epidemic. Agric Meteorol 132:20–27 http://dx.doi.org/10.1016/j.agrformet.2005.06.007.
71. Schmale DG, Ross SD, Fetters TL, Tallapragada P, Wood-Jones AK, Dingus B. 2012. Isolates of Fusarium graminearum collected 40–320 meters above ground level cause Fusarium head blight in wheat and produce trichothecene mycotoxins. Aerobiologia 28:1–11 http://dx.doi.org/10.1007/s10453-011-9206-2.
72. Muñoz J, Felicísimo ÁM, Cabezas F, Burgaz AR, Martínez I. 2004. Wind as a long-distance dispersal vehicle in the Southern Hemisphere. Science 304:1144–1147 http://dx.doi.org/10.1126/science.1095210.
73. Bowden J, Gregory PH, Johnson CG. 1971. Possible wind transport of coffee leaf rust across the Atlantic Ocean. Nature 229:500–501 http://dx.doi.org/10.1038/229500b0.
74. Purdy LH. 1985. Introduction of sugarcane rust into the Americas and its spread to Florida. Plant Dis 69:689 http://dx.doi.org/10.1094/PD-69-689.
75. Unterseher M, Jumpponen A, Opik M, Tedersoo L, Moora M, Dormann CF, Schnittler M. 2011. Species abundance distributions and richness estimations in fungal metagenomics: lessons learned from community ecology. Mol Ecol 20:275–285 http://dx.doi.org/10.1111/j.1365-294X.2010.04948.x.
76. Tedersoo L, Anslan S, Bahram M, Põlme S, Riit T, Liiv I, Kõljalg U, Kisand V, Nilsson H, Hildebrand F, Bork P, Abarenkov K. 2015. Shotgun metagenomes and multiple primer pair-barcode combinations of amplicons reveal biases in metabarcoding analyses of fungi. MycoKeys 10:1–43 http://dx.doi.org/10.3897/mycokeys.10.4852.
77. Peay KG, Schubert MG, Nguyen NH, Bruns TD. 2012. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21:4122–4136 http://dx.doi.org/10.1111/j.1365-294X.2012.05666.x.
78. Prospero JM, Blades E, Mathison G, Naidu R. 2015. Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia 21:1–19 http://dx.doi.org/10.1007/s10453-004-5872-7.
79. Paugam R, Wooster M, Freitas S, Val Martin M. 2016. A review of approaches to estimate wildfire plume injection height within large-scale atmospheric chemical transport models. Atmos Chem Phys 16:907–925 http://dx.doi.org/10.5194/acp-16-907-2016.
80. Mims SA, Mims FM III. 2004. Fungal spores are transported long distances in smoke from biomass fires. Atmos Environ 38:651–655 http://dx.doi.org/10.1016/j.atmosenv.2003.10.043.
81. de Resende AS, Xavier RP, de Oliveira OC, Urquiaga S, Alves BJR, Boddey RM. 2006. Long-term effects of pre-harvest burning and nitrogen and vinasse applications on yield of sugar cane and soil carbon. Plant Soil 281:339–351 http://dx.doi.org/10.1007/s11104-005-4640-y.
82. Rämä T, Nordén J, Davey ML, Mathiassen GH, Spatafora JW, Kauserud H. 2014. Fungi ahoy! Diversity on marine wooden substrata in the high North. Fungal Ecol 8:46–58 http://dx.doi.org/10.1016/j.funeco.2013.12.002.
83. Johansen S, Hytteborn H. 2001. A contribution to the discussion of biota dispersal with drift ice and driftwood in the North Atlantic. J Biogeogr 28:105–115 http://dx.doi.org/10.1046/j.1365-2699.2001.00532.x.
84. Hellmann L, Tegel W, Eggertsson Ó, Schweingruber FH, Blanchette R, Kirdyanov A, Gärtner H, Büntgen U. 2013. Tracing the origin of Arctic driftwood. J Geophys Res D Atmospheres 118:68–76 http://dx.doi.org/10.1002/jgrg.20022.
85. Hayward J, Hynson NA. 2014. New evidence of ectomycorrhizal fungi in the Hawaiian Islands associated with the endemic host Pisonia sandwicensis Nyctaginaceae. Fungal Ecol 12:62–69 http://dx.doi.org/10.1016/j.funeco.2014.09.001.
86. Nicolson TH, Johnston C. 1979. Mycorrhiza in the Gramineae. III. Glomusfasiculatus as the endophyte of pioneer grasses in maritime dunes. Trans Br Mycol Soc 72:261–268 http://dx.doi.org/10.1016/S0007-1536(79)80041-8.
87. Koske RE, Gemma JN. 1990. VA mycorrhizae in strand vegetation of Hawaii: evidence for long-distance codispersal of plants and fungi. Am J Bot 77:466–474 http://dx.doi.org/10.2307/2444380.
88. Moncalvo J-M, Buchanan PK. 2008. Molecular evidence for long distance dispersal across the Southern Hemisphere in the Ganoderma applanatum-australe species complex (Basidiomycota). Mycol Res 112:425–436 http://dx.doi.org/10.1016/j.mycres.2007.12.001.
89. Pang KL, Vrijmoed LLP, Jones EBG. 2013. Genetic variation within the cosmopolitan aquatic fungus Lignincola laevis (Microascales, Ascomycota). Org Divers Evol 13:301–309 http://dx.doi.org/10.1007/s13127-013-0132-8.
90. Wong MKM, Goh TK, Hodgkiss IJ, Hyde KD, Ranghoo VM, Tsui CKM, Ho WH, Wong WSW, Yuen TK. 1998. Role of fungi in freshwater ecosystems. Biodivers Conserv 7:1187–1206 http://dx.doi.org/10.1023/A:1008883716975.
91. Chauvet E, Cornut J, Sridhar KR, Selosse MA, Bärlocher F. 2016. Beyond the water column: aquatic hyphomycetes outside their preferred habitat. Fungal Ecol 19:112–127 http://dx.doi.org/10.1016/j.funeco.2015.05.014.
92. Goh TK, Hyde KD. 1996. Biodiversity of freshwater fungi. J Ind Microbiol Biotechnol 17:328–345 http://dx.doi.org/10.1007/BF01574764.
93. Colgan W III, Claridge AW. 2002. Mycorrhizal effectiveness of Rhizopogon spores recovered from faecal pellets of small forest-dwelling mammals. Mycol Res 106:314–320 http://dx.doi.org/10.1017/S0953756202005634.
94. D’Alva T, Lara C, Estrada-Torres A, Castillo-Guevara C. 2007. Digestive responses of two omnivorous rodents (Peromyscus maniculatus and P. alstoni) feeding on epigeous fungus (Russula occidentalis). J Comp Physiol B 177:707–712 http://dx.doi.org/10.1007/s00360-007-0188-x.
95. Greif MD, Currah RS. 2007. Patterns in the occurrence of saprophytic fungi carried by arthropods caught in traps baited with rotted wood and dung. Mycologia 99:7–19 http://dx.doi.org/10.1080/15572536.2007.11832595.
96. Rudolphi J. 2009. Ant-mediated dispersal of asexual moss propagules. Bryologist 112:73–79 http://dx.doi.org/10.1639/0007-2745-112.1.73.
97. de Vega C, Arista M, Ortiz PL, Herrera CM, Talavera S. 2011. Endozoochory by beetles: a novel seed dispersal mechanism. Ann Bot 107:629–637 http://dx.doi.org/10.1093/aob/mcr013.
98. Piattoni F, Amicucci A, Iotti M, Ori F, Stocchi V, Zambonelli A. 2014. Viability and morphology of Tuber aestivum spores after passage through the gut of Sus scrofa. Fungal Ecol 9:52–60 http://dx.doi.org/10.1016/j.funeco.2014.03.002.
99. Weseloh RM. 2003. Short and long range dispersal in the gypsy moth Lepidoptera: Lymantriidae fungal pathogen, Entomophaga maimaiga Zygomycetes: Entomophthorales. Environ Entomol 32:111–122 http://dx.doi.org/10.1603/0046-225X-32.1.111.
100. Venkatesh MV, Joshi KR, Harjai SC, Ramdeo IN. 1975. Aspergillosis in desert locust (Schistocerka gregaria Forsk). Mycopathologia 57:135–138 http://dx.doi.org/10.1007/BF00551419.
101. Whitehill JG, Lehman JS, Bonello P. 2007. Ips pini (Curculionidae: Scolytinae) is a vector of the fungal pathogen, Sphaeropsis sapinea (Coelomycetes), to Austrian pines, Pinus nigra (Pinaceae). Environ Entomol 36:114–120 http://dx.doi.org/10.1603/0046-225X(2007)36[114:IPCSIA]2.0.CO;2.
102. Roets F, Wingfield MJ, Crous PW, Dreyer LL. 2009. Fungal radiation in the Cape Floristic region: an analysis based on Gondwanamyces and Ophiostoma. Mol Phylogenet Evol 51:111–119 http://dx.doi.org/10.1016/j.ympev.2008.05.041.
103. Aylward J, Dreyer LL, Steenkamp ET, Wingfield MJ, Roets F. 2014. Panmixia defines the genetic diversity of a unique arthropod-dispersed fungus specific to Protea flowers. Ecol Evol 4:3444–3455 http://dx.doi.org/10.1002/ece3.1149.
104. Koch FH, Smith WD. 2008. Spatio-temporal analysis of Xyleborus glabratus (Coleoptera: Curculionidae [corrected] Scolytinae) invasion in eastern U.S. forests. Environ Entomol 37:442–452 http://dx.doi.org/10.1093/ee/37.2.442.
105. Lara C, Ornelas JF. 2003. Hummingbirds as vectors of fungal spores in Moussonia deppeana (Gesneriaceae): taking advantage of a mutualism? Am J Bot 90:262–269 http://dx.doi.org/10.3732/ajb.90.2.262.
106. Barton CE, Phalen DN, Snowden KF. 2003. Prevalence of microsporidian spores shed by asymptomatic lovebirds: evidence for a potential emerging zoonosis. J Avian Med Surg 17:197–202 http://dx.doi.org/10.1647/2002-011.
107. Lallo MA, Calábria P, Milanelo L. 2012. Encephalitozoon and Enterocytozoon (microsporidia) spores in stool from pigeons and exotic birds: microsporidia spores in birds. Vet Parasitol 190:418–422 http://dx.doi.org/10.1016/j.vetpar.2012.06.030.
108. Alfonzo A, Francesca N, Sannino C, Settanni L, Moschetti G. 2013. Filamentous fungi transported by birds during migration across the Mediterranean sea. Curr Microbiol 66:236–242 http://dx.doi.org/10.1007/s00284-012-0262-9.
109. Puechmaille SJ, Wibbelt G, Korn V, Fuller H, Forget F, Mühldorfer K, Kurth A, Bogdanowicz W, Borel C, Bosch T, Cherezy T, Drebet M, Görföl T, Haarsma AJ, Herhaus F, Hallart G, Hammer M, Jungmann C, Le Bris Y, Lutsar L, Masing M, Mulkens B, Passior K, Starrach M, Wojtaszewski A, Zöphel U, Teeling EC. 2011. Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS One 6:e19167 http://dx.doi.org/10.1371/journal.pone.0019167.
110. Hayes MA. 2012. The Geomyces fungi: ecology and distribution. Bioscience 62:819–823 http://dx.doi.org/10.1525/bio.2012.62.9.7.
111. Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, La Marca E, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, Sánchez-Azofeifa GA, Still CJ, Young BE. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167 http://dx.doi.org/10.1038/nature04246.
112. Whittaker K, Vredenburg V. 2011. An Overview of Chytridiomycosis. Amphibiaweb, Berkeley, CA.
113. Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, Garner TWJ, Weaver G, Group TBM, Fisher MC. 2013. Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus complex. Mol Ecol 21:281–299.
114. Weldon C, du Preez LH, Hyatt AD, Muller R, Speare R. 2004. Origin of the amphibian chytrid fungus. Emerg Infect Dis 10:2100–2105 http://dx.doi.org/10.3201/eid1012.030804.
115. Ron SR. 2005. Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica 37:209–221 http://dx.doi.org/10.1111/j.1744-7429.2005.00028.x.
116. Swei A, Rowley JJL, Rödder D, Diesmos MLL, Diesmos AC, Briggs CJ, Brown R, Cao TT, Cheng TL, Chong RA, Han B, Hero JM, Hoang HD, Kusrini MD, Le DTT, McGuire JA, Meegaskumbura M, Min MS, Mulcahy DG, Neang T, Phimmachak S, Rao DQ, Reeder NM, Schoville SD, Sivongxay N, Srei N, Stöck M, Stuart BL, Torres LS, Tran DTA, Tunstall TS, Vieites D, Vredenburg VT. 2011. Is chytridiomycosis an emerging infectious disease in Asia? PLoS One 6:e23179 http://dx.doi.org/10.1371/journal.pone.0023179.
117. Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, Kidd M, Blaser MJ, Graham DY, Vacher S, Perez-Perez GI, Yamaoka Y, Mégraud F, Otto K, Reichard U, Katzowitsch E, Wang X, Achtman M, Suerbaum S. 2003. Traces of human migrations in Helicobacter pylori populations. Science 299:1582–1585 http://dx.doi.org/10.1126/science.1080857.
118. Araujo A, Reinhard KJ, Ferreira LF, Gardner SL. 2008. Parasites as probes for prehistoric human migrations? Trends Parasitol 24:112–115 http://dx.doi.org/10.1016/j.pt.2007.11.007.
119. Breurec S, Guillard B, Hem S, Brisse S, Dieye FB, Huerre M, Oung C, Raymond J, Tan TS, Thiberge JM, Vong S, Monchy D, Linz B. 2011. Evolutionary history of Helicobacter pylori sequences reflect past human migrations in Southeast Asia. PLoS One 6:e22058 http://dx.doi.org/10.1371/journal.pone.0022058.
120. Slatkin M. 1987. Gene flow and the geographic structure of natural populations. Science 236:787–792 http://dx.doi.org/10.1126/science.3576198.
121. Fisher MC, Koenig GL, White TJ, San-Blas G, Negroni R, Alvarez IG, Wanke B, Taylor JW. 2001. Biogeographic range expansion into South America by Coccidioides immitis mirrors New World patterns of human migration. Proc Natl Acad Sci USA 98:4558–4562 http://dx.doi.org/10.1073/pnas.071406098.
122. Goebel T, Waters MR, O’Rourke DH. 2008. The late Pleistocene dispersal of modern humans in the Americas. Science 319:1497–1502 http://dx.doi.org/10.1126/science.1153569.
123. Legras J-L, Merdinoglu D, Cornuet J-M, Karst F. 2007. Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol Ecol 16:2091–2102 http://dx.doi.org/10.1111/j.1365-294X.2007.03266.x.
124. Milgroom MG, Lipari SE. 1995. Population differentiation in the chestnut blight fungus, Cryphonectria parasitica, in eastern North America. Phytopathology 85:155–160 http://dx.doi.org/10.1094/Phyto-85-155.
125. Milgroom MG, Wang K, Zhou Y, Lipari SE, Kaneko S. 1996. Intercontinental population structure of the chestnut blight fungus, Cryphonectria parasitica. Mycologia 88:179–190 http://dx.doi.org/10.2307/3760921.
126. Brasier CM, Buck KW. 2001. Rapid evolutionary changes in a globally invading fungal pathogen Dutch elm disease. Biol Invasions 3:223–233 http://dx.doi.org/10.1023/A:1015248819864.
127. Et-touil K, Bernier L, Beaulieu J, Bérubé JA, Hopkin A, Hamelin RC. 1999. Genetic structure of Cronartium ribicola populations in eastern Canada. Phytopathology 89:915–919 http://dx.doi.org/10.1094/PHYTO.1999.89.10.915.
128. Vellinga EC, Wolfe BE, Pringle A. 2009. Global patterns of ectomycorrhizal introductions. New Phytol 181:960–973 http://dx.doi.org/10.1111/j.1469-8137.2008.02728.x.
129. Stukenbrock EH, Banke S, McDonald BA. 2006. Global migration patterns in the fungal wheat pathogen Phaeosphaeria nodorum. Mol Ecol 15:2895–2904 http://dx.doi.org/10.1111/j.1365-294X.2006.02986.x.
130. Hovmøller MS, Yahyaoui AH, Milus EA, Justesen AF. 2008. Rapid global spread of two aggressive strains of a wheat rust fungus. Mol Ecol 17:3818–3826 http://dx.doi.org/10.1111/j.1365-294X.2008.03886.x.
131. Linde CC, Zala M, McDonald BA. 2009. Molecular evidence for recent founder populations and human-mediated migration in the barley scald pathogen Rhynchosporium secalis. Mol Phylogenet Evol 51:454–464 http://dx.doi.org/10.1016/j.ympev.2009.03.002.
132. Gough FJ, Lee TS. 1985. Moisture effects on the discharge and survival of conidia of Septoria tritici. Phytopathology 75:180–182 http://dx.doi.org/10.1094/Phyto-75-180.
133. Pringle A, Brenner MP, Fritz JA, Roper M, Seminara A. 2017. Reaching the wind: boundary layer escape as a constraint on ascomycete spore shooting, p •••–•••. In Dighton J, White JF (ed), The Fungal Community: Its Organization and Role in the Ecosystem, 4th ed. CRC Press, Boca Raton, FL.
134. Roper M, Seminara A, Bandi MM, Cobb A, Dillard HR, Pringle A. 2010. Dispersal of fungal spores on a cooperatively generated wind. Proc Natl Acad Sci USA 107:17474–17479 http://dx.doi.org/10.1073/pnas.1003577107.
135. Jenkins DG, Brescacin CR, Duxbury CV, Elliott JA, Evans JA, Grablow KR, Hillegass M, Lyon BN, Metzger GA, Olandese ML, Pepe D, Silvers G, Suresch HN, Thompson TN, Trexler CM, Williams GE, Williams NC, Williams SE. 2007. Does size matter for dispersal distance? Glob Ecol Biogeogr 16:415–425 http://dx.doi.org/10.1111/j.1466-8238.2007.00312.x.
136. Fritz JA, Seminara A, Roper M, Pringle A, Brenner MP. 2013. A natural O-ring optimizes the dispersal of fungal spores. J R Soc Interface 10:20130187 http://dx.doi.org/10.1098/rsif.2013.0187.
137. Kauserud H, Colman JE, Ryvarden L. 2008. Relationship between basidiospore size, shape and life history characteristics: a comparison of polypores. Fungal Ecol 1:19–23 http://dx.doi.org/10.1016/j.funeco.2007.12.001.
138. Kauserud H, Heegaard E, Halvorsen R, Boddy L, Høiland K, Stenseth NC. 2011. Mushroom’s spore size and time of fruiting are strongly related: is moisture important? Biol Lett 7:273–276 http://dx.doi.org/10.1098/rsbl.2010.0820.
139. Norros V, Rannik U, Hussein T, Petäjä T, Vesala T, Ovaskainen O. 2014. Do small spores disperse further than large spores? Ecology 95:1612–1621 http://dx.doi.org/10.1890/13-0877.1.
140. Hussein T, Norros V, Hakala J, Petäjä T, Aalto PP, Rannik Ü, Vesala T, Ovaskainen O. 2013. Species traits and inertial deposition of fungal spores. J Aerosol Sci 61:81–98 http://dx.doi.org/10.1016/j.jaerosci.2013.03.004.
141. Reponen T, Willeke K, Ulevicius V, Reponen A, Grinshpun SA. 1996. Effect of relative humidity on the aerodynamic diameter and respiratory deposition of fungal spores. Atmos Environ 30:3967–3974 http://dx.doi.org/10.1016/1352-2310(96)00128-8.
142. Tesmer J, Schnittler M. 2007. Sedimentation velocity of myxomycete spores. Mycol Prog 6:229–234 http://dx.doi.org/10.1007/s11557-007-0539-8.
143. Roper M, Pepper RE, Brenner MP, Pringle A. 2008. Explosively launched spores of ascomycete fungi have drag-minimizing shapes. Proc Natl Acad Sci USA 105:20583–20588 http://dx.doi.org/10.1073/pnas.0805017105.
144. Wong LT, Yu HC, Mui KW, Chan WY. 2015. Drag constants for common indoor bioaerosols. Indoor Built Environ 24:401–413 http://dx.doi.org/10.1177/1420326X13515897.
145. Halbwachs H, Brandl R, Bässler C. 2015. Spore wall traits of ectomycorrhizal and saprotrophic agarics may mirror their distinct lifestyles. Fungal Ecol 17:197–204 http://dx.doi.org/10.1016/j.funeco.2014.10.003.
146. Pringle A, Vellinga E, Peay K. 2015. The shape of fungal ecology: does spore morphology give clues to a species’ niche? Fungal Ecol 17:213–216 http://dx.doi.org/10.1016/j.funeco.2015.04.005.
147. Trunov M, Trakumas S, Willeke K, Grinshpun SA, Reponen T. 2001. Collection of bioaerosol particles by impaction: effect of fungal spore agglomeration and bounce. Aerosol Sci Technol 34:490–498 http://dx.doi.org/10.1080/02786820121411.
148. Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K, Elluru SR, Clavaud C, Paris S, Brakhage AA, Kaveri SV, Romani L, Latgé JP. 2009. Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460:1117–1121 http://dx.doi.org/10.1038/nature08264.
149. Fisher MC, Gow NAR, Gurr SJ. 2016. Tackling emerging fungal threats to animal health, food security and ecosystem resilience. Philos Trans R Soc Lond B Biol Sci 371:20160332 http://dx.doi.org/10.1098/rstb.2016.0332.
150. Whiteford JR, Spanu PD. 2002. Hydrophobins and the interactions between fungi and plants. Mol Plant Pathol 3:391–400 http://dx.doi.org/10.1046/j.1364-3703.2002.00129.x.
151. Huffman JA, Prenni AJ, DeMott PJ, Pöhlker C, Mason RH, Robinson NH, Fröhlich-Nowoisky J, Tobo Y, Després VR, Garcia E, Gochis DJ, Harris E, Müller-Germann I, Ruzene C, Schmer B, Sinha B, Day DA, Andreae MO, Jimenez JL, Gallagher M, Kreidenweis SM, Bertram AK, Pöschl U. 2013. High concentrations of biological aerosol particles and ice nuclei during and after rain. Atmos Chem Phys 13:6151–6164 http://dx.doi.org/10.5194/acp-13-6151-2013.
152. Iannone R, Chernoff DI, Pringle A, Martin ST, Bertram AK. 2011. The ice nucleation ability of one of the most abundant types of fungal spores found in the atmosphere. Atmos Chem Phys 11:1191–1201 http://dx.doi.org/10.5194/acp-11-1191-2011.
153. Hassett MO, Fischer MWF, Money NP. 2015. Mushrooms as rainmakers: how spores act as nuclei for raindrops. PLoS One 10:e0140407 http://dx.doi.org/10.1371/journal.pone.0140407. [PubMed]
154. Morris CE, Sands DC, Glaux C, Samsatly J, Asaad S, Moukahel AR, Gonçalves FLT, Bigg EK. 2013. Urediospores of rust fungi are ice nucleation active at > −10 °C and harbor ice nucleation active bacteria. Atmos Chem Phys 13:4223–4233 http://dx.doi.org/10.5194/acp-13-4223-2013.
155. Fröhlich-Nowoisky J, Hill TCJ, Pummer BG, Yordanova P, Franc GD, Pöschl U. 2015. Ice nucleation activity in the widespread soil fungus Mortierella alpina. Biogeosciences 12:1057–1071 http://dx.doi.org/10.5194/bg-12-1057-2015.
156. Pope FD. 2010. Pollen grains are efficient cloud condensation nuclei. Environ Res Lett 5:44015 http://dx.doi.org/10.1088/1748-9326/5/4/044015.
157. Buller AHR. 1909. Researches on Fungi. Longmans, Green and Co, London, United Kingdom. http://dx.doi.org/10.5962/bhl.title.5397
158. Ingold CT. 1971. Fungal Spores: Their Liberation and Dispersal. Clarendon Press, Oxford, United Kingdom.
159. Pringle A, Patek SN, Fischer M, Stolze J, Money NP. 2005. The captured launch of a ballistospore. Mycologia 97:866–871 http://dx.doi.org/10.1080/15572536.2006.11832777.
160. Sache I. 2000. Short-distance dispersal of wheat rust spores. Agronomie 20:757–767 http://dx.doi.org/10.1051/agro:2000102.
161. McCartney HA, Bainbridge A. 1987. Deposition of Erysiphe graminis conidia on a barley crop. J Phytopathol 118:243–257 http://dx.doi.org/10.1111/j.1439-0434.1987.tb00453.x.
162. Lacey M, West J. 2006. The Air Spora: a Manual for Catching and Identifying Airborne Biological Particles. Springer, Dordrecht, The Netherlands. http://dx.doi.org/10.1007/978-0-387-30253-9
163. Leite B, Navaez D, Marois J, Wright D. 2007. Clumping of Phakopsora pachyrhizi urediniospores and its significance in spore biology. Phytopathology 97:S63.
164. Richard F, Glass NL, Pringle A. 2012. Cooperation among germinating spores facilitates the growth of the fungus, Neurospora crassa. Biol Lett 8:419–422 http://dx.doi.org/10.1098/rsbl.2011.1141.
165. Nix-Stohr S, Moshe R, Dighton J. 2008. Effects of propagule density and survival strategies on establishment and growth: further investigations in the phylloplane fungal model system. Microb Ecol 55:38–44 http://dx.doi.org/10.1007/s00248-007-9248-8.
166. Maddison AC, Manners JG. 1972. Sunlight and viability of cereal rust uredospores. Trans Br Mycol Soc 59:429–443 http://dx.doi.org/10.1016/S0007-1536(72)80124-4.
167. Fernando WG, Miller JD, Seaman WL, Seifert K, Paulitz TC. 2000. Daily and seasonal dynamics of airborne spores of Fusarium graminearum and other Fusarium species sampled over wheat plots. Can J Bot 78:497–505 http://dx.doi.org/10.1139/b00-027.
168. Park S, Chen Z-Y, Chanda AK, Schneider RW, Hollier CA. 2008. Viability of Phakopsora pachyrhizi urediniospores under simulated southern Louisiana winter temperature conditions. Plant Dis 92:1456–1462 http://dx.doi.org/10.1094/PDIS-92-10-1456.
169. Borg-Karlson A-K, Englund FO, Unelius CR. 1994. Dimethyl oligosulphides, major volatiles released from Sauromatum guttatum and Phallus impudicus. Phytochemistry 35:321–323 http://dx.doi.org/10.1016/S0031-9422(00)94756-3.
170. Pelusio F, Nilsson T, Montanarella L, Tilio R, Larsen B, Facchetti S, Madsen J. 1995. Headspace solid-phase microextraction analysis of volatile organic sulfur compounds in black and white truffle aroma. J Agric Food Chem 43:2138–2143.
171. Sleeman DP, Jones P, Cronin JN. 1997. Investigations of an association between the stinkhorn fungus and badger setts. J Nat Hist 31:983–992 http://dx.doi.org/10.1080/00222939700770481.
172. Johnson SD, Jürgens A. 2010. Convergent evolution of carrion and faecal scent mimicry in fly-pollinated angiosperm flowers and a stinkhorn fungus. S Afr J Bot 76:796–807 http://dx.doi.org/10.1016/j.sajb.2010.07.012.
173. Schigel DS. 2012. Fungivory and host associations of Coleoptera: a bibliography and review of research approaches. Mycology 3:258–272.
174. Dressaire E, Yamada L, Song B, Roper M. 2016. Mushrooms use convectively created airflows to disperse their spores. Proc Natl Acad Sci USA 113:2833–2838 http://dx.doi.org/10.1073/pnas.1509612113.
175. Savage D, Barbetti MJ, MacLeod WJ, Salam MU, Renton M. 2012. Seasonal and diurnal patterns of spore release can significantly affect the proportion of spores expected to undergo long-distance dispersal. Microb Ecol 63:578–585 http://dx.doi.org/10.1007/s00248-011-9949-x.
176. Troutt C, Levetin E. 2001. Correlation of spring spore concentrations and meteorological conditions in Tulsa, Oklahoma. Int J Biometeorol 45:64–74 http://dx.doi.org/10.1007/s004840100087.
177. Burch M, Levetin E. 2002. Effects of meteorological conditions on spore plumes. Int J Biometeorol 46:107–117 http://dx.doi.org/10.1007/s00484-002-0127-1.
178. Grinn-Gofroń A, Strzelczak A. 2013. Changes in concentration of Alternaria and Cladosporium spores during summer storms. Int J Biometeorol 57:759–768 http://dx.doi.org/10.1007/s00484-012-0604-0.
179. Dales RE, Cakmak S, Judek S, Dann T, Coates F, Brook JR, Burnett RT. 2003. The role of fungal spores in thunderstorm asthma. Chest 123:745–750 http://dx.doi.org/10.1378/chest.123.3.745.
180. Lieberman BS. 2005. Geobiology and paleobiogeography: tracking the coevolution of the Earth and its biota. Palaeogeogr Palaeoclimatol Palaeoecol 219:23–33 http://dx.doi.org/10.1016/j.palaeo.2004.10.012.
181. Mao K, Milne RI, Zhang L, Peng Y, Liu J, Thomas P, Mill RR, Renner SS. 2012. Distribution of living Cupressaceae reflects the breakup of Pangea. Proc Natl Acad Sci USA 109:7793–7798 http://dx.doi.org/10.1073/pnas.1114319109.
182. De Queiroz A. 2014. The Monkey’s Voyage: How Improbable Journeys Shaped the History of Life. Basic Books, Philadelphia, PA.
183. Gutiérrez EE, Boria RA, Anderson RP. 2014. Can biotic interactions cause allopatry? Niche models, competition, and distributions of South American mouse opossums. Ecography 37:741–753 http://dx.doi.org/10.1111/ecog.00620.
184. Lichtwardt RW. 1995. Biogeography and fungal systematics. Can J Bot 73(S1):731–737 http://dx.doi.org/10.1139/b95-316.
185. Moyersoen B, Beever RE, Martin F. 2003. Genetic diversity of Pisolithus in New Zealand indicates multiple long-distance dispersal from Australia. New Phytol 160:569–579 http://dx.doi.org/10.1046/j.1469-8137.2003.00908.x.
186. Coetzee MPA, Bloomer P, Wingfield MJ, Wingfield BD. 2011. Paleogene radiation of a plant pathogenic mushroom. PLoS One 6:e28545 http://dx.doi.org/10.1371/journal.pone.0028545.
187. Theodoro RC, Teixeira MM, Felipe MSS, Paduan KS, Ribolla PM, San-Blas G, Bagagli E. 2012. Genus paracoccidioides: species recognition and biogeographic aspects. PLoS One 7:e37694 http://dx.doi.org/10.1371/journal.pone.0037694.
188. Davis MA. 2009. Invasion Biology. Oxford University Press, Oxford, United Kingdom.
189. Nucci M, Marr KA. 2005. Emerging fungal diseases. Clin Infect Dis 41:521–526 http://dx.doi.org/10.1086/432060.
190. Schneider RW, Hollier CA, Whitam HK, Palm ME, McKemy JM, Hernández JR, Levy L, DeVries-Paterson R. 2005. First report of soybean rust caused by Phakopsora pachyrhizi in the continental United States. Plant Dis 89:774.1. doi:10.1094/PD-89-0774A.
191. Yorinori JT, Paiva WM, Frederick RD, Costamilan LM, Bertagnolli PF, Hartman GE, Godoy CV, Nunes J Jr. 2005. Epidemics of soybean rust Phakopsora pachyrhizi in Brazil and Paraguay from 2001 to 2003. Plant Dis 89:675–677 http://dx.doi.org/10.1094/PD-89-0675.
192. Goellner K, Loehrer M, Langenbach C, Conrath U, Koch E, Schaffrath U. 2010. Phakopsora pachyrhizi, the causal agent of Asian soybean rust. Mol Plant Pathol 11:169–177 http://dx.doi.org/10.1111/j.1364-3703.2009.00589.x.
193. Werth S, Wagner HH, Gugerli F, Holderegger R, Csencsics D, Kalwij JM, Scheidegger C. 2006. Quantifying dispersal and establishment limitation in a population of an epiphytic lichen. Ecology 87:2037–2046 http://dx.doi.org/10.1890/0012-9658(2006)87[2037:QDAELI]2.0.CO;2.
194. Johnson DA, Ball TA, Hess WM. 1999. Image analysis of urediniospores that infect Mentha. Mycologia 91:1016–1020 http://dx.doi.org/10.2307/3761633.
195. Marleau J, Dalpé Y, St-Arnaud M, Hijri M. 2011. Spore development and nuclear inheritance in arbuscular mycorrhizal fungi. BMC Evol Biol 11:51 http://dx.doi.org/10.1186/1471-2148-11-51.
196. Wittmaack K, Wehnes H, Heinzmann U, Agerer R. 2005. An overview on bioaerosols viewed by scanning electron microscopy. Sci Total Environ 346:244–255 http://dx.doi.org/10.1016/j.scitotenv.2004.11.009.
197. Piepenbring M, Bauer R, Oberwinkler F. 1998. Teliospores of smut fungi teliospore walls and the development of ornamentation studied by electron microscopy. Protoplasma 204:170–201 http://dx.doi.org/10.1007/BF01280323.
198. Carvalho CR, Fernandes RC, Carvalho GMA, Barreto RW, Evans HC. 2011. Cryptosexuality and the genetic diversity paradox in coffee rust, Hemileia vastatrix. PLoS One 6:e26387 http://dx.doi.org/10.1371/journal.pone.0026387.
199. Dixon LJ, Castlebury LA, Aime MC, Glynn NC, Comstock JC. 2010. Phylogenetic relationships of sugarcane rust fungi. Mycol Prog 9:459–468 http://dx.doi.org/10.1007/s11557-009-0649-6.
200. Tzean SS, Hsieh WH, Chang TT, Wu SH, Ho HM. 2015. Mycobiota Taiwanica, 3rd ed. National Taiwan University, TaiPei, Taiwan.
201. Liu N, Gong G, Zhang M, Zhou Y, Chen Z, Yang J, Chen H, Wang X, Lei Y, Liu K. 2012. Over-summering of wheat powdery mildew in Sichuan Province, China. Crop Prot 34:112–118 http://dx.doi.org/10.1016/j.cropro.2011.12.011.
202. Leslie JF, Summerell BA (ed). 2006. The Fusarium Laboratory Manual. Blackwell, Ames, IA. http://dx.doi.org/10.1002/9780470278376
203. Stover RH. 1963. Leaf spot of bananas caused by Mycosphaerella musicola: associated ascomycetous fungi. Can J Bot 41:1481–1485 http://dx.doi.org/10.1139/b63-128.
204. Qandah IS, del Río Mendoza LE. 2011. Temporal dispersal patterns of Sclerotinia sclerotiorum ascospores during canola flowering. Can J Plant Pathol 33:159–167 http://dx.doi.org/10.1080/07060661.2011.554878.
205. Aylor DE. 1992. Release of Venturia inaequalis ascospores during unsteady rain: relationship to spore transport and deposition. Phytopathology 82:532–540 http://dx.doi.org/10.1094/Phyto-82-532.
206. Vincenot L, Nara K, Sthultz C, Labbé J, Dubois M-P, Tedersoo L, Martin F, Selosse M-A. 2012. Extensive gene flow over Europe and possible speciation over Eurasia in the ectomycorrhizal basidiomycete Laccaria amethystina complex. Mol Ecol 21:281–299 http://dx.doi.org/10.1111/j.1365-294X.2011.05392.x.
207. Aylor DE, Taylor G. 1983. Escape of Peronospora tabacina spores from a field of diseased tobacco plants. Phytopathology 73:525–529 http://dx.doi.org/10.1094/Phyto-73-525.
208. Simmonds NW. 1994. Some speculative calculations of the dispersal of sugarcane smut disease. Sugar Cane 1:2–5.
209. Isard SA, Gage SH, Comtois P, Russo JM. 2005. Principles of the atmospheric pathway for invasive species applied to soybean rust. Bioscience 55:851–861 http://dx.doi.org/10.1641/0006-3568(2005)055[0851:POTAPF]2.0.CO;2.
210. Anikster Y, Eilam T, Bushnell WR, Kosman E. 2005. Spore dimensions of Puccinia species of cereal hosts as determined by image analysis. Mycologia 97:474–484 http://dx.doi.org/10.1080/15572536.2006.11832823.
211. Ali S, Gladieux P, Leconte M, Gautier A, Justesen AF, Hovmøller MS, Enjalbert J, de Vallavieille-Pope C. 2014. Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici. PLoS Pathog 10:e1003903 http://dx.doi.org/10.1371/journal.ppat.1003903.
212. Lawrence D. 2008. Batrachochytrium dendrobatidis: Chytrid Disease. Oregon State University, Corvallis, OR.
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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0047-2016
2017-07-14
2017-09-26

Abstract:

Dispersal is a fundamental biological process, operating at multiple temporal and spatial scales. Despite an increasing understanding of fungal biodiversity, most research on fungal dispersal focuses on only a small fraction of species. Thus, any discussion of the dispersal dynamics of fungi as a whole is problematic. While abundant morphological and biogeographic data are available for hundreds of species, researchers have yet to integrate this information into a unifying paradigm of fungal dispersal, especially in the context of long-distance dispersal (LDD). Fungal LDD is mediated by multiple vectors, including meteorological phenomena (e.g., wind and precipitation), plants (e.g., seeds and senesced leaves), animals (e.g., fur, feathers, and gut microbiomes), and in many cases humans. In addition, fungal LDD is shaped by both physical constraints on travel and the ability of spores to survive harsh environments. Finally, fungal LDD is commonly measured in different ways, including by direct capture of spores, genetic comparisons of disconnected populations, and statistical modeling and simulations of dispersal data. To unify perspectives on fungal LDD, we propose a synthetic three-part definition that includes (i) an identification of the source population and a measure of the concentration of source inoculum and (ii) a measured and/or modeled dispersal kernel. With this information, LDD is defined as (iii) the distance found within the dispersal kernel beyond which only 1% of spores travel.

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Figures

Image of FIGURE 1
FIGURE 1

A framework for understanding fungal LDD.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0047-2016
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Image of FIGURE 2
FIGURE 2

Sizes of fungal spores and other airborne particles. Some species are wind dispersed (e.g., ), while others have other means of dispersal (e.g., ). The smallest plant seed, , the pollen grains of and , and a glomerospore of the arbuscular mycorrhizal are provided for comparison. Species labeled with an asterisk are not fungi.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0047-2016
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Image of FIGURE 3
FIGURE 3

To integrate the disparate approaches used to describe and measure fungal LDD, we propose a synthetic three-part definition building on the general framework presented by Nathan ( 1 , 28 ). A description of fungal LDD should include (i) identification of a source population and measure of source inoculum concentration (e.g., the number of spores in a single rust pustule), (ii) a measured and/or modeled dispersal kernel, and (iii) a measure of the distance, based on the dispersal kernel, past which only 1% of spores travel. Adopting a standard approach would mitigate the confusion caused by differing definitions and measurements of LDD and facilitate comparisons among the dispersal kernels of different species. In the illustration, the blue and red dispersal kernels demonstrate idealized kernels for two hypothetical species. LDD is defined per species at distances A and B, respectively—the distance beyond which only 1% of spores travel. We next used our approach with real dispersal data of (measured as the number of resistant lesions per square meter of banana leaf measured from a source to 1,000 m) ( 52 ), (measured as the recovery rate of ascospores of a unique clone released from a source to 1,000 m) ( 58 ), and (measured as the proportion of DNA from snow samples identical to an isolated source of soredia up to a distance of 40 m [ 193 ]) to estimate dispersal kernels and identify LDD for each species. We smoothed the published data to estimate an approximate dispersal kernel, and the distance beyond which 1% of spores traveled was found by integrating the area under each kernel from 0 m to the distance at which 99% of spores had been captured. Although both and are capable of dispersing to approximately 1,000 m, the proportion of spores that fit our definition of LDD varies considerably, because LDD is defined past 714 m for and past 250 m for . A holistic comparison of the two dispersal kernels suggests that different dynamics will shape the effective reach of each species. The dispersal kernel of illustrates how truncated experimental setups can impact measures of LDD. At the furthest collection point (40 m), a large proportion of samples tested positive, and the best dispersal kernel that can be modeled from the data ( 193 ) provides what is likely an underestimate of LDD, at approximately 39 m (15% of the positive samples collected at 0 m were detected). Ideally, the tail end of a modeled dispersal kernel should very closely approach a horizontal line at = 0.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0047-2016
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Image of FIGURE 4
FIGURE 4

A phylogram of genetic distances among 15 geographic populations of . The fact that geographically distant populations of are grouped together, e.g., Uruguayan populations are grouped with Algerian and Syrian populations, likely suggests movement mediated by humans. infects one of the most traded agricultural products (wheat), and its ascospores cannot survive prolonged exposure to, e.g., dry air ( 183 ). Data adapted from Zhan et al. ( 64 ); similar clustering of geographically distant populations is found from data on ( 129 ), ( 131 ), and ( 60 ).

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0047-2016
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Image of FIGURE 5
FIGURE 5

Images of various fungal spores. Basidiospores of (brown powder) next to seeds of (semicircles) and sugar crystals (white cubes). Urediniospores of (Fig. 1 of reference 194 ). Conidia of and . is a putative long-distance disperser, while (10× in size) is not (courtesy of Steve Jordan). Glomerospore of (Fig. 5i of reference 195 ). Conidium of (Fig. 5c of reference 196 ). Teliospore of (Fig. 9 of reference 197 ). Urediniospore of (Fig. 1e of reference 198 ). Urediniospore size, shape, and ornamentation of (Fig. 1d of reference 199 ). Zoospores of chytrid ( 200 ). Ascospores of ( 200 ). Sporangiospores of var. ( 200 ). Basidiospores of still on soredia ( 200 ). Conidia of the aquatic ascomycete (Fig. 66 of reference 92 ).

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0047-2016
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Image of FIGURE 6
FIGURE 6

Comparing spore sizes to reported maximum dispersal distances. Spore volume in square micrometers is measured on the left-hand vertical axis, and spore Q-ratio (the ratio of spore length to width) is measured on the right. Data points were calculated from the parameters listed in Table 1 . There is a poor correlation between approximate maximum dispersal distance and both average spore volumes (R = 0.0167, = 0.5568) and Q-ratios (R = 0.1113, = 0.1198). The lack of any correlation likely reflects inconsistent definitions and measurements of LDD, rather than any biological reality.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0047-2016
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Image of FIGURE 7
FIGURE 7

Images of spore dispersal structures among fungi. Basidiospores of carried vertically by evaporative airflows from mushroom cap (Fig. 1e of reference 174 ). Hypogeous spore body of (Wikimedia Commons Creative Commons Attribution-Share Alike 3.0 Unported [WC]). Sporangium of releasing sporangiospores (courtesy of Andrii Gryganskyi). mushroom (Doug Collins, WC). Synchronous spore release from apothecia (Fig. 1b of reference 135 ). Asci of ( 200 ). Apothecia of ( 200 ). Typical gilled agaric mushroom with gills to increase surface area of spore-producing tissue (WC).

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0047-2016
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Tables

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TABLE 1

Spore parameters for putative long-distance dispersers

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0047-2016

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