Abstract
The agricultural use of commercial “biofertilizers” containing arbuscular mycorrhizal (AM) fungi, obligate symbionts that help plants take up nutrients, has resulted in the global introduction of AM fungi to non-native environments. Despite their growing use and evidence for endemism among AM fungi, the risk of AM fungi becoming invasive through “biofertilizer” application has not been studied in the context of general invasion theory. Understanding their dispersal by multiple vectors and in different environments is key to understanding how quickly they could spread. In this review, we consider the risk of invasion by commercial AM fungi in terms of a theoretical framework. We propose traits that make an isolate good for use as a commercial product, such competitiveness and high sporulation rate, may also increase invasiveness.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbott LK, Robson AD (1985) The effect of soil-pH on the formation of VA mycorrhizas by 2 species of Glomus. Aust J Soil Res 23:253–261
Allen MF (1987) Re-establishment of mycorrhizas on Mount St. Helens: migration vectors. Trans Br Mycol Soc 88:413–441. https://doi.org/10.1016/S0007-1536(87)80019-0
Allen MF, MacMahon JA (1988) Direct VA mycorrhizal inoculation of colonizing plants by pocket Gophers (Thomomys talpoides) on Mount St. Helens. Mycologia 80:754–756
Allen MF, MacMahon JA, Andersen DC (1984) Reestablishment of endogonaceae on Mount St. Helens: survival of residuals. Mycologia 76:1031–1038
Allen MF, Hipps LE, Wooldridge GL (1989) Wind dispersal and subsequent establishment of VA mycorrhizai fungi across a successional arid landscape. Landsc Ecol 2:165–171
Andow DA, Kareiva PM, Levin SA, Okubo A (1990) Spread of invading organisms. Landsc Ecol 4:177–188. https://doi.org/10.1007/BF00132860
Angelard C, Tanner CJ, Fontanillas P, Niculita-Hirzel H, Masclaux F, Sanders IR (2014) Rapid genotypic change and plasticity in arbuscular mycorrhizal fungi is caused by a host shift and enhanced by segregation. ISME J 8:284–294. https://doi.org/10.1038/ismej.2013.154
Baas-Becking L (1934) Geobiologie of inleiding tot de milieukunde. Van Stockkum & Zoon, The Hague
Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, Jhala YV, Pierce MA, Rahmani AR, Fonseca DM, Fleischer RC (2006) Global phylogeographic limits of Hawaii’s avian malaria. Proc R Soc B Biol Sci 273:2935–2944. https://doi.org/10.1098/rspb.2006.3671
Berruti A, Lumini E, Balestrini R, Bianciotto V (2016a) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1–13. https://doi.org/10.3389/fmicb.2015.01559
Berruti A, Lumini E, Bianciotto V (2016b) AMF components from a microbial inoculum fail to colonize roots and lack soil persistence in an arable maize field. Symbiosis. https://doi.org/10.1007/s13199-016-0442-7
Bever JD, Wang M (2005) Hyphal fusion and multigenomic structure. Nature 433:2004–2005. https://doi.org/10.1038/nature03294
Bever JD, Schultz PA, Pringle A, Morton JB (2001) Arbuscular mycorrhizal fungi: more diverse than meets the eye, and the ecological tale of why. Bioscience 51:923–932. https://doi.org/10.1641/0006-3568(2001)051
Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478. https://doi.org/10.1016/j.tree.2010.05.004
Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339. https://doi.org/10.1016/j.tree.2011.03.023
Blanke V, Renker C, Wagner M, Füllner K, Held M, Kuhn AJ, Buscot F (2005) Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytol 166:981–992. https://doi.org/10.1111/j.1469-8137.2005.01374.x
Brasier CM (2000) Intercontinental spread and continuing evolution of the dutch elm disease pathogens. In: Dunn CP (ed) The elms: breeding, conservation, and disease management. Kluwer Academic Publishers, Boston, pp 61–72
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77
Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733. https://doi.org/10.1038/nature02322
Camargo-Ricalde SL (2002) Dispersal, distribution, and establishment of mycorrhizal fungi: a review. Boletín la Soc Botánica México 71:33–44
Chaudhary VB, Lau MK, Johnson NC (2008) Macroecology of microbes—biogeography of the Glomeromycota. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer, New York, pp 529–563
Cordell D, White S (2013) Sustainable phosphorus measures: strategies and technologies for achieving phosphorus security. Agronomy 3:86–116. https://doi.org/10.3390/agronomy3010086
Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305. https://doi.org/10.1016/j.gloenvcha.2008.10.009
Corkidi L, Allen EB, Merhaut D, Allen MF, Downer J, Bohn J, Evans M (2004) Assessing the infectivity of commercial mycorrhizal inoculants in plant nursery conditions. J Environ Hortic 22:149–154
Davison J, Ainsaar L, Burla S et al (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973. https://doi.org/10.5061/dryad.2m15n
de Bruyn LAL, Conacher AJ (1994) The bioturbation activity of ants in agricultural and naturally vegetated habitats in semi-arid environments. Aust J Soil Res 32:555–570
de la Providencia IE, Nadimi M, Beaudet D, Morales GR, Hijri M (2013) Detection of a transient mitochondrial DNA heteroplasmy in the progeny of crossed genetically divergent isolates of arbuscular mycorrhizal fungi. New Phytol 200:211–221
de Vries FT, Thébault E, Liiri M et al (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci U S A 110:14296–14301. https://doi.org/10.1073/pnas.1305198110
Declerck S, Strullu DG, Plenchette C (1996) In vitro mass-production of the arbuscular mycorrhizal fungus, Glomus versiforme, associated with Ri T-DNA transformed carrot roots. Mycol Res 100:1237–1242. https://doi.org/10.1016/S0953-7562(96)80186-9
Egan C, Li DW, Klironomos J (2014) Detection of arbuscular mycorrhizal fungal spores in the air across different biomes and ecoregions. Fungal Ecol 12:26–31. https://doi.org/10.1016/j.funeco.2014.06.004
Egerton-Warburton LM, Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–496
Farmer MJ, Li X, Feng G, Zhao B, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V, van Tuinen D (2007) Molecular monitoring of field-inoculated AMF to evaluate persistence in sweet potato crops in China. Appl Soil Ecol 35:599–609. https://doi.org/10.1016/j.apsoil.2006.09.012
Faye A, Dalpé Y, Ndung’u-Magiroi K, Jefwa J, Ndoye I, Diouf M, Lesueur D (2013) Evaluation of commercial arbuscular mycorrhizal inoculants. Can J Plant Sci 93:1201–1208. https://doi.org/10.4141/cjps2013-326
Feurtey A, Cornille A, Shykoff JA, Snirc A, Giraud T (2016) Crop-to-wild gene flow and its fitness consequences for a wild fruit tree: towards a comprehensive conservation strategy of the wild apple in Europe. Evol Appl 10:180–188. https://doi.org/10.1111/eva.12441
Fitter AH, Garbaye J (1994) Interactions between mycorrhizal fungi and other soil organisms. Plant Soil 159:123–132
Food and Agriculture Association of the United Nations (2017) World fertilizer outlook to 2020. FAO.
Friese CF, Allen MF (1991) The spread of VA mycorrhizal fungal hyphae in the soil: inoculum types and external hyphal architecture. Mycologia 83:409–418
Gange AC (1993) Translocation of mycorrhizal fungi by earthworms during early succession. Soil Biol Biochem 25:1021–1026
Gianinazzi S, Vosátka M (2004) Inoculum of arbuscular mycorrhizal fungi for production systems: science meets business. Can J Bot 82:1264–1271. https://doi.org/10.1139/b04-072
Goto BT, Maia LC (2005) Sporocarpic species of arbuscular mycorrhizal fungi (Glomeromycota), with a new report from Brazil. Acta Bot Bras 19:633–637. https://doi.org/10.1590/S0102-33062005000300025
Göttlich E, Van Der Lubbe W, Lange B et al (2002) Fungal flora in groundwater-derived public drinking water. Int J Hyg Environ Health 205:269–279
Graham JH, Leonard RT, Menge JA (1982) Interaction of light intensity and soil temperature with phosphorus inhibition of vesicular-arbuscular mycorrhiza formation. New Phytol 91:683–690
Griebler C, Lueders T (2009) Microbial biodiversity in groundwater ecosystems. Freshw Biol 54:649–677. https://doi.org/10.1111/j.1365-2427.2008.02013.x
Grünwald NJ, Garbelotto M, Goss EM, Heungens K, Prospero S (2012) Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends Microbiol 20:131–138
Harinikumar KM, Bagyaraj DJ (1994) Potential of earthworms, ants, millipedes, and termites for dissemination of vesicular-arbuscular mycorrhizal fungi in soil. Biol Fertil Soils 18:115–118. https://doi.org/10.1007/BF00336456
Harner MJ, Piotrowski JS, Lekberg Y, Stanford JA, Rillig MC (2009) Heterogeneity in mycorrhizal inoculum potential of flood-deposited sediments. Aquat Sci 71:331–337. https://doi.org/10.1007/s00027-009-9198-y
Hart MM, Reader RJ, Klironomos JN (2003) Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends Ecol Evol 18:418–423. https://doi.org/10.1016/S0169-5347(03)00127-7
Hart MM, Antunes PM, Abbott LK (2017) Unknown risks to soil biodiversity from commercial fungal inoculants. Nat Ecol Evol. https://doi.org/10.1038/s41559-017-0115
Hastings A, Cuddington K, Davies KF, Dugaw CJ, Elmendorf S, Freestone A, Harrison S, Holland M, Lambrinos J, Malvadkar U, Melbourne BA, Moore K, Taylor C, Thomson D (2005) The spatial spread of invasions: new developments in theory and evidence. Ecol Lett 8:91–101. https://doi.org/10.1111/j.1461-0248.2004.00687.x
Haygood R, Ives AR, Andow DA (2003) Consequences of recurrent gene flow from crops to wild relatives. Proc R Soc B 270:1879–1886. https://doi.org/10.1098/rspb.2003.2426
Hazard C, Gosling P, van der Gast CJ, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. ISME J 7:498–508. https://doi.org/10.1038/ismej.2012.127
Hernádi I, Sasvári Z, Albrechtová J, Posta K (2012) Arbuscular mycorrhizal inoculant increases yield of spice pepper and affects the indigenous fungal community in the field. HortScience 47:603–606
Hijri M, Sanders IR (2005) Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 433:160–163. https://doi.org/10.1038/nature03158.1
Ingold C, Hudson H (1993) Dispersal in Fungi. The biology of fungi, sixth. Springer, Dordrecht, pp 119–131
Janos DP, Sahley CT, Emmons LH (1995) Rodent dispersal of vesicular-arbuscular mycorrhizal fungi in amazonian Peru. Ecology 76:1852–1858
Jin H, Germida JJ, Walley FL (2013) Impact of arbuscular mycorrhizal fungal inoculants on subsequent arbuscular mycorrhizal fungi colonization in pot-cultured field pea (Pisum sativum L.). Mycorrhiza 23:45–59. https://doi.org/10.1007/s00572-012-0448-9
Johnson D, Vandenkoornhuyse PJ, Leake JR et al (2003) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515. https://doi.org/10.1046/j.1469-8137.2003.00938.x
Kanzler D, Buzina W, Paulitsch A et al (2007) Occurrence and hygienic relevance of fungi in drinking water. Mycoses 51:165–169. https://doi.org/10.1111/j.1439-0507.2007.01454.x
Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303. https://doi.org/10.1016/j.soilbio.2011.07.012
Klironomos JN, Kendrick WB (1996) Palatability of microfungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae. Biol Fertil Soils 21:43–52
Klironomos JN, Moutoglis P (1999) Colonization of nonmycorrhizal plants by mycorrhizal neighbours as influenced by the collembolan, Folsomia candida. Biol Fertil Soils 29:277–281
Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR (2004) High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proc Natl Acad Sci 101:2369–2374. https://doi.org/10.1073/pnas.0306441101
Koch AM, Antunes PM, Barto EK, Cipollini D, Mummey DL, Klironomos J (2011) The effects of arbuscular mycorrhizal (AM) fungal and garlic mustard introductions on native AM fungal diversity. Biol Invasions 13:1627–1639. https://doi.org/10.1007/s10530-010-9920-7
Koch AM, Antunes PM, Maherali H, Hart MM, Klironomos JN (2017) Evolutionary asymmetry in the arbuscular mycorrhizal symbiosis: conservatism in fungal morphology does not predict host plant growth. New Phytol 214:1330–1337. https://doi.org/10.1111/nph.14465
Köhl L, Lukasiewicz CE, Van der Heijden MGA (2016) Establishment and effectiveness of inoculated arbuscular mycorrhizal fungi in agricultural soils. Plant, Cell Environ 39:136–146. https://doi.org/10.1111/pce.12600
Kot M, Lewis MA, van den Driessche P (1996) Dispersal data and the spread of invading organisms. Ecology 77:2027–2042
Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745–748. https://doi.org/10.1038/414745a
Lee KK, Reddy MV, Wani SP, Trirnurtulu N (1996) Vesicular-arbuscular mycorrhizal fungi in earthworm casts and surrounding soil in relation to soil management of a semi-arid tropical Alfisol. Appl Soil Ecol 3:177–181
Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? a meta analysis of studies published between 1988 and 2003. New Phytol 168:189–204
Litchman E (2010) Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol Lett 13:1560–1572. https://doi.org/10.1111/j.1461-0248.2010.01544.x
Malloch D, Blackwell M (1992) Dispersal of Fungal Diaspores. In: Carroll G, Wicklow D (eds) The fungal community: its organization and role in the ecosystem, second. Marcel Dekker Inc, New York, pp 147–172
Malusá E, Vassilev N (2014) A contribution to set a legal framework for biofertilisers. Appl Microbiol Biotechnol 98:6599–6607. https://doi.org/10.1007/s00253-014-5828-y
Mangan SA, Adler GH (2000) Consumption of arbuscular mycorrhizal fungi by terrestrial and arboreal small mammals in a panamanian cloud forest. J Mammal 81:563–570
Mangan SA, Adler GH (2002) Seasonal dispersal of arbuscular mycorrhizal fungi by spiny rats in a neotropical forest. Oecologia 131:587–597. https://doi.org/10.1007/s00442-002-0907-7
Martiny JBH, Bohannan BJM, Brown JH et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112. https://doi.org/10.1038/nrmicro1341
Maser C, Trappe JM, Nussbaum RA (1978) Fungal-small mammal interrelationships with emphasis on oregon coniferous forests. Ecology 59:799–809
McGonigle TP (1995) The significance of grazing on fungi in nutrient cycling. Can J Bot 73:S1370–S1376
McIlveen WD, Cole HJ (1976) Spore dispersal of Endogonaceae by worms, ants, wasps, and birds. Can J Bot 54:1486–1489
Mummey DL, Antunes PM, Rillig MC (2009) Arbuscular mycorrhizal fungi pre-inoculant identity determines community composition in roots. Soil Biol Biochem 41:1173–1179. https://doi.org/10.1016/j.soilbio.2009.02.027
Nielsen KB, Kjøller R, Bruun HH, Schnoor TK, Rosendahl S (2016) Colonization of new land by arbuscular mycorrhizal fungi. Fungal Ecol 20:22–29. https://doi.org/10.1016/j.funeco.2015.10.004
Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, van der Heijden M, Sieverding E (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42:724–738. https://doi.org/10.1016/j.soilbio.2010.01.006
Oehl F, Laczko E, Oberholzer H, Jansa J, Egli S (2017) Diversity and biogeography of arbuscular mycorrhizal fungi in agricultural soils. Biol Fertil Soils. https://doi.org/10.1007/s00374-017-1217-x
Ohsowski BM, Zaitsoff PD, Öpik M, Hart MM (2014) Where the wild things are: looking for uncultured Glomeromycota. New Phytol 204:171–179. https://doi.org/10.1111/nph.12894
Öpik M, Zobel M, Cantero JJ et al (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430. https://doi.org/10.1007/s00572-013-0482-2
Pellegrino E, Turrini A, Gamper HA, Cafà G, Bonari E, Young JPW, Giovanetti M (2012) Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components. New Phytol 194:810–822. https://doi.org/10.1111/j.1469-8137.2012.04090.x
Pereira VJ, Basílio MC, Fernandes D, Domingues M, Paiva JM, Benoliel MJ, Crespo MT, San Ramão MV (2009) Occurrence of filamentous fungi and yeasts in three different drinking water sources. Water Res 43:3813–3819. https://doi.org/10.1016/j.watres.2009.05.024
Powell C (1979) Spread of mycorrhizal fungi through soil. New Zeal J Agric Res 22:335–339. https://doi.org/10.1080/00288233.1979.10430756
Pringle A, Adams RI, Cross HB, Bruns TD (2009) The ectomycorrhizal fungus Amanita phalloides was introduced and is expanding its range on the west coast of North America. Mol Ecol 18:817–833. https://doi.org/10.1111/j.1365-294X.2008.04030.x
Purin S, Morton JB (2011) In situ analysis of anastomosis in representative genera of arbuscular mycorrhizal fungi. Mycorrhiza 21:505–514. https://doi.org/10.1007/s00572-010-0356-9
Reddell P, Spain AV (1991) Earthworms as vectors of viable propagules of mycorrhizal fungi. Soil Biol Biochem 23:767–774
Reddell P, Spain AV, Hopkins M (1997) Dispersal of spores of mycorrhizal fungi in scats of native mammals in tropical forests of Northeastern Australia. Biotropica 29:184–192
Ricciardi A, Blackburn TM, Carlton JT et al (2017) Invasion science: a horizon scan of emerging challenges and opportunities. Trends Ecol Evol 32:464–474. https://doi.org/10.1016/j.tree.2017.03.007
Richardson DM, Pysek P, Rejmánek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107
Rodriguez A, Sanders IR (2014) The role of community and population ecology in applying mycorrhizal fungi for improved food security. ISME J 9:1053–1061. https://doi.org/10.1038/ismej.2014.207
Ropars J, Toro K, Noel J, Pelin A, Charron P, Farinelli L, Marton T, Krüger M, Kuchs J, Brachmann A, Corradi N (2016) Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi. Nat Microbiol. https://doi.org/10.1038/nmicrobiol.2016.33
Rosendahl S, McGee P, Morton JB (2009) Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Mol Ecol 18:4316–4329. https://doi.org/10.1111/j.1365-294X.2009.04359.x
Rúa MA, Antoninka A, Antunes PM, Chaudhary VJ, Gehring C, Lamit LJ, Piculell BJ, Bever JD, Zabinski C, Meadow JF, Lajeunesse MJ, Milligan BG, Karst J, Hoeksema JD (2016) Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16:1–16. https://doi.org/10.1186/s12862-016-0698-9
Ryan MH, Graham JH (2002) Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant Soil 244:263–271. https://doi.org/10.1023/A:1020207631893
Sanders IR, Croll D (2010) Arbuscular mycorrhiza: the challenge to understand the genetics of the fungal partner. Annu Rev Genet 44:271–292. https://doi.org/10.1146/annurev-genet-102108-134239
Schechter SP, Bruns TD (2013) A common garden test of host-symbiont specificity supports a dominant role for soil type in determining AMF assemblage structure in collinsia sparsiflora. PLoS One. https://doi.org/10.1371/journal.pone.0055507
Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, Pringle A (2006) The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol Lett 9:501–515. https://doi.org/10.1111/j.1461-0248.2006.00910.x
Simberloff D, Parker IM, Windle PN (2005) Introduced species policy, management, and future research needs. Front Ecol Environ 3:12–20
Skellam JG (1951) Random dispersal in theoretical populations. Biometrika 38:196–218
Smith SE, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York
Šobotník J, Jirošová A, Hanus R (2010) Chemical warfare in termites. J Insect Physiol 56:1012–1021. https://doi.org/10.1016/j.jinsphys.2010.02.012
St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1996) Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus GIomus intraradices in an in vitro system in the absence of host roots. Mycol Res 100:328–332. https://doi.org/10.1016/S0953-7562(96)80164-X
Stürmer SL, Morton JB (1997) Developmental patterns defining morphological characters in spores of four species in Glomus. Mycologia 89:72–81
Sýkorová Z, Börstler B, Zvolenská S, Fehrer J, Gryndler M, Vosátka M, Redecker D (2012) Long-term tracing of Rhizophagus irregularis isolate BEG140 inoculated on Phalaris arundinacea in a coal mine spoil bank, using mitochondrial large subunit rDNA markers. Mycorrhiza 22:69–80. https://doi.org/10.1007/s00572-011-0375-1
Symanczik S, Courty PE, Boller T, Wiemken A, Al-Yahya’ei MN (2015) Impact of water regimes on an experimental community of four desert arbuscular mycorrhizal fungal (AMF) species, as affected by the introduction of a non-native AMF species. Mycorrhiza 25:639–647. https://doi.org/10.1007/s00572-015-0638-3
Tarbell TJ, Koske RE (2007) Evaluation of commercial arbuscular mycorrhizal inocula in a sand/peat medium. Mycorrhiza 18:51–56. https://doi.org/10.1007/s00572-007-0152-3
Thirkell TJ, Charters MD, Elliott AJ, Sait SM, Field KJ (2017) Are mycorrhizal fungi our sustainable saviours? considerations for achieving food security. J Ecol 105:921–929. https://doi.org/10.1111/1365-2745.12788
Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Bécard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young JPW, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. PNAS 110:20117–20122
Tommerup IC (1982) Airstream fractionation of vesicular-arbuscular mycorrhizal fungi: concentration and enumeration of propagules. Appl Environ Microbiol 44:533–539
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72
van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157:569–578
van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x
Verbruggen E, van der Heijden MGA, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109. https://doi.org/10.1111/j.1469-8137.2012.04348.x
Warner NJ, Allen MF, MacMahon JA (1987) Dispersal agents of vesicular-arbuscular mycorrhizal fungi in a disturbed arid ecosystem. Mycologia 79:721–730
Werner GDA, Kiers ET (2015) Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytol 205:1515–1524. https://doi.org/10.1111/nph.13092
Wicklow DT, Yocom DH (1982) Effect of larval grazing by Lycoriella mali (Diptera: Sciaridae) on species abundance of coprophilous fungi. Trans Br Mycol Soc 78:29–32. https://doi.org/10.1016/S0007-1536(82)80073-9
Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666
Zaharick J, Beck H, Beauchamp V (2015) An experimental test of Epi- and Endozoochory of Arbuscular Mycorrhizal fungi spores by small mammals in a Maryland forest. Northeast Nat 22:163–177
Acknowledgements
We are grateful to two anonymous reviewers who provided feedback on an earlier version of this manuscript. This work was supported by grants from the NSERC Discovery Program and AAFC Growing Forward 2 to M.M.H., and a NSERC CGS-M Award to C.N.T.
Author information
Authors and Affiliations
Contributions
CNT led the writing with substantial contributions from MMH, and the ideas presented herein were developed together.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Thomsen, C.N., Hart, M.M. Using invasion theory to predict the fate of arbuscular mycorrhizal fungal inoculants. Biol Invasions 20, 2695–2706 (2018). https://doi.org/10.1007/s10530-018-1746-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-018-1746-8