Abstract
The inability to associate with local species may constrain the spread of mutualists arriving to new habitats, but the fates of introduced, microbial mutualists are largely unknown. The deadly poisonous ectomycorrhizal fungus Amanita phalloides (the death cap) is native to Europe and introduced to the East and West Coasts of North America. By cataloging host associations across the two continents, we record dramatic changes in specificity among the three ranges. On the East Coast, where the fungus is restricted in its distribution, it associates almost exclusively with pines, which are rarely hosts of A. phalloides in its native range. In California, where the fungus is widespread and locally abundant, it associates almost exclusively with oaks, mirroring the host associations observed in Europe. The most common host of the death cap in California is the endemic coast live oak (Quercus agrifolia), and the current distribution of A. phalloides appears constrained within the distribution of Q. agrifolia. In California, host shifts to native plants are also associated with a near doubling in the resources allocated to sexual reproduction and a prolonged fruiting period; mushrooms are twice as large as they are elsewhere and mushrooms are found throughout the year. Host and niche shifts are likely to shape the continuing range expansion of A. phalloides and other ectomycorrhizal fungi introduced across the world.
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References
Amundson R, Austin AT, Schuur EAG, Yoo K, Matzek V, Kendall C et al. (2003). Global patterns of the isotopic composition of soil and plant nitrogen. Global Biogeochem Cycles 17: 1031.
Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P . (2004). Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19: 535–544.
Andrew C, Lilleskov EA . (2009). Productivity and community structure of ectomycorrhizal fungal sporocarps under increased atmospheric CO2 and O3 . Ecol Lett 12: 813–822.
Brown JL, Morales V, Summers K . (2009). Home range size and location in relation to reproductive resources in poison frogs (Dendrobatidae): a Monte Carlo approach using GIS data. Anim Behav 77: 547–554.
Beug MW, Shaw M, Cochran KW . (2006). Thirty-plus years of mushroom poisoning: summary of the approximately 2,000 reports in the NAMA Case registry. McIlvainea 16: 47–68.
Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ . (2004). Is invasion success explained by the enemy release hypothesis? Ecol Lett 7: 721–733.
Courtecuisse R, Duhem B . (1994). Guide des Champignons de France et d’Europe. Delachaux & Niestlé: Lausanne.
Dickie IA, Bolstridge N, Cooper JA, Peltzer DA . (2010). Co-invasion by Pinus and its mycorrhizal fungi. New Phytol 187: 475–484.
Diefendorf AF, Mueller KE, Wing SL, Koch PL, Freeman KH . (2010). Global patterns in leaf 13C discrimination and implications for studies of past and future climate. Proc Natl Acad Sci USA 107: 5738–5743.
Diez J . (2005). Invasion biology of Australian ectomycorrhizal fungi introduced with eucalypt plantations into the Iberian Peninsula. Biol Invasions 7: 3–15.
Fox LR, Morrow PA . (1981). Specialization: species property or local phenomenon? Science 211: 887–893.
Gilbert GS, Gorospe J, Ryvarden L . (2008). Host and habitat preferences of polypore fungi in micronesian tropical flooded forests. Mycol Res 112: 674–680.
Guidot A, Gryta H, Gourbiere F, Debaud JC, Marmeisse R . (2002). Forest habitat characteristics affect balance between sexual reproduction and clonal propagation of the ectomycorrhizal mushroom Hebeloma cylindrosporum. Oikos 99: 25–36.
Hobbie EA, Colpaert JV . (2003). Nitrogen availability and colonization by mycorrhizal fungi correlate with nitrogen isotope patterns in plants. New Phytol 157: 115–126.
Hobbie EA, Weber NS, Trappe JM . (2001). Mycorrhizal vs. saprotrophic status of fungi: the isotopic evidence. New Phytol 150: 601–610.
Hobbie JE, Hobbie EA . (2006). 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in arctic tundra. Ecology 87: 816–822.
Högberg P, Plamboeck AH, Taylor AFS, Fransson PMA . (1999). Natural 13C abundance reveals trophic status of fungi and host-origin of carbon in mycorrhizal fungi in mixed forests. Proc Natl Acad Sci USA 96: 8534–8539.
Jairus T, Mpumba R, Chinoya S, Tedersoo L . (2011). Invasion potential and host shifts of Australian and African ectomycorrhizal fungi in mixed eucalypt plantations. New Phytol 192: 179–187.
Karst J, Marczak L, Jones MD, Turkington R . (2008). The mutualism-parasitism continuum in ectomycorrhizas: a quantitative assessment using meta-analysis. Ecology 89: 1032–1042.
Kennedy PG, Izzo AD, Bruns TD . (2003). There is high potential for the formation of common mycorrhizal networks between understorey and canopy trees in a mixed evergreen forest. J Ecol 91: 1071–1080.
Kiers ET, Rousseau RA, West SA, Denison RF . (2003). Host sanctions and the legume-rhizobium mutualism. Nature 425: 78–81.
Kuikka K, Härmä E, Markkola A, Rautio P, Roitto M, Saikkonen K et al. (2003). Severe defoliation of Scots pine reduces reproductive investment by ectomycorrhizal symbionts. Ecology 84: 2051–2061.
Litchman E . (2010). Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol Lett 13: 1560–1572.
Manos PS, Zhou ZK, Cannon CH . (2001). Systematics of Fagaceae: phylogenetic tests of reproductive trait evolution. Int J Plant Sci 162: 1361–1379.
Marshall JD, Brooks JR, Lajtha K . (2007) Sources of variation in the stable isotopic composition of plants. In: Michener R, Lajtha K (eds), Stable Isotopes in Ecology and Environmental Science 2nd edn. Blackwell Publishing: Malden, MA, pp 22–60.
Markkola A, Kuikka K, Rautio P, Härmä E, Roitto M, Tuomi J . (2004). Defoliation increases carbon limitations in ectomycorrhizal symbiosis of Betula pubescens. Oecologia 140: 234–240.
Massicotte HB, Molina R, Tackaberry LE, Smith JE, Amaranthus MP . (1999). Diversity and host specificity of ectomycorrhizal fungi retrieved from three adjacent forest sites by five host species. Can J Bot 77: 1053–1076.
Mitchell CE, Agrawak AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN et al. (2006). Biotic interactions and plant invasions. Ecol Lett 9: 726–740.
Molina R, Massicotte J, Trappe JM . (1992). Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. In: Allen A (ed.), Mycorrhizal Functioning. Chapman and Hall: New York, pp 357–420.
Morris MH, Smith ME, Rizzo DM, Rejmanek M, Bledsoe CS . (2008). Contrasting ectomycorrhizal fungal communities on the roots of co-occurring oaks (Quercus spp.) in a California woodland. New Phytol 178: 167–176.
Oono R, Denison RF, Kiers ET . (2009). Controlling the reproductive fate of rhizobia: how universal are legume sanctions? New Phytol 183: 967–979.
Pringle A, Vellinga EC . (2006). Last chance to know? Using literature to explore the biogeography and invasion biology of the death cap mushroom Amanita phalloides (vaill. ex fr.: Fr.) link. Biol Invasions 8: 1131–1144.
Pringle A, Adams RI, Cross HB, Bruns TD . (2009a). The ectomycorrhizal fungus Amanita phalloides was introduced and is expanding its range on the west coast of North America. Mol Ecol 18: 817–833.
Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN . (2009b). Mycorrhizal symbioses and plant invasions. Ann Rev Ecol Evol Syst 40: 699–715.
Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M . (2000). Plant invasions - the role of mutualisms. Biol Rev Camb Philos Soc 75: 65–93.
Sato H, Yumoto T, Murakami N . (2007). Cryptic species and host specificity in the ectomycorrhizal genus Strobilomyces (Strobilomycetaceae). Am J Bot 94: 1630–1641.
Saylor HM . (1984). A. phalloides in California: this preliminary report suggests that it is a relative newcomer to the state. Mushroom Magazine 2: 40–42.
Saari SK, Campbell CD, Russell J, Alexander IJ, Anderson IC . (2005). Pine microsatellite markers allow roots and ectomycorrhizas to be linked to individual trees. New Phytol 165: 295–304.
Schmit JP . (2002). Tradeoffs between reproduction and mycelium production in the unit-restricted decomposer Coprinus cinereus. Mycologia 94: 40–48.
Slippers B, Stenlid J, Wingfield MJ . (2005). Emerging pathogens: fungal host jumps following anthropogenic introduction. Trends Ecol Evol 20: 420–421.
Smith ME, Douhan GW, Fremier AK, Rizzo DM . (2009). Are true multihost fungi the exception or the rule? Dominant ectomycorrhizal fungi on Pinus sabiniana differ from those on co-occurring Quercus species. New Phytol 182: 295–299.
Smith SE, Read DJ . (1997). Mycorrhizal Symbiosis 2nd edn. Academic Press: London.
Stukenbrock EH, McDonald BA . (2008). The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 46: 75–100.
Suits NS, Denning AS, Berry JA, Still CJ, Kaduk K, Miller JB, Baker IT . (2005). Simulation of carbon isotope discrimination of the terrestrial biosphere. Global Biogeochem Cycles 19: GB1017.
Tanghe LJ . (1983). Spread of Amanita phalloides in North America. McIllvainea 6: 4–8.
Tanghe LJ, Simons DM . (1973). Amanita phalloides in the Eastern United States. Mycologia 65: 99–108.
Taylor AFS, Fransson PM, Högberg P, Högberg MN, Plamboeck AH . (2003). Species level patterns in 13C and 15N abundance of ectomycorrhizal and saprotrophic fungal sporocarps. New Phytol 159: 757–774.
Thompson JN . (1994). The Coevolutionary Process. University of Chicago Press: Chicago.
Torchin ME, Mitchell CE . (2004). Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2: 183–190.
United States Geological Survey (2006). Digital representations of three species range maps from “Atlas of United States Trees” by Elbert L. Little, Jr. (and other publications). Available at: http://esp.cr.usgs.gov/data/atlas/little/.Accessed February 5, 2009.
van der Putten WH, Klironomos JN, Wardle DA . (2007). Microbial ecology of biological invasions. ISME J 1: 28–37.
Vázquez DP . (2005). Exploring the relationship between niche breadth and invasion success. In: Cadotte MW, McMahon SM, Fukami T (eds), Conceptual Ecology and Invasions Biology: Reciprocal Approaches to Nature. Springer: Dordrecht, pp 307–322.
Vellinga EC, Wolfe BE, Pringle A . (2009). Global patterns of ectomycorrhizal introductions. New Phytol 181: 960–973.
Wolfe BE, Richard F, Cross HB, Pringle A . (2010). Distribution and abundance of the introduced ectomycorrhizal fungus Amanita phalloides in North America. New Phytol 185: 803–816.
Woolhouse MEJ, Haydon DT, Antia R . (2005). Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol Evol 20: 238–244.
Yahr R, Vilgalys R, DePriest PT . (2006). Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytologist 171: 847–860.
Acknowledgements
Darvin Deshazer, Jason Hoeksema, Jason Hollinger, Joel Horman, Susan Hopkins, June Johnston, Marion Kyde, Jan Lindgren, Rich Moll, Dan Nicholson, Ron Pastorino, Bob Peabody, David Rust, Paul Sadowski, Douglas Smith, Walt Sturgeon, Steven Trudell, Rod Tulloss, Debbie Veiss, Else Vellinga, Peter Werner and Nathan Wilson provided collections or assistance with locating A. phalloides populations. Hope Jahren provided support with the stable isotope analysis. Matthew Smith and Noah Whiteman helped with earlier drafts of this manuscript. The study was funded by the New England Botanical Club, The Arnold Arboretum of Harvard University, the Mycological Society of America and the US National Science Foundation.
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Wolfe, B., Pringle, A. Geographically structured host specificity is caused by the range expansions and host shifts of a symbiotic fungus. ISME J 6, 745–755 (2012). https://doi.org/10.1038/ismej.2011.155
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