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Dispersal of Arbuscular Mycorrhizal Fungi: Evidence and Insights for Ecological Studies

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Abstract

Dispersal is a critical ecological process that modulates gene flow and contributes to the maintenance of genetic and taxonomic diversity within ecosystems. Despite an increasing global understanding of the arbuscular mycorrhizal (AM) fungal diversity, distribution and prevalence in different biomes, we have largely ignored the main dispersal mechanisms of these organisms. To provide a geographical and scientific overview of the available data, we systematically searched for the direct evidence on the AM fungal dispersal agents (abiotic and biotic) and different propagule types (i.e. spores, extraradical hyphae or colonized root fragments). We show that the available data (37 articles) on AM fungal dispersal originates mostly from North America, from temperate ecosystems, from biotic dispersal agents (small mammals) and AM fungal spores as propagule type. Much lesser evidence exists from South American, Asian and African tropical systems and other dispersers such as large-bodied birds and mammals and non-spore propagule types. We did not find strong evidence that spore size varies across dispersal agents, but wind and large animals seem to be more efficient dispersers. However, the data is still too scarce to draw firm conclusions from this finding. We further discuss and propose critical research questions and potential approaches to advance the understanding of the ecology of AM fungi dispersal.

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References

  1. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528

    Article  Google Scholar 

  2. Nathan R (2006) Long-distance dispersal of plants. Science 313:786–788. https://doi.org/10.1126/science.1124975

    Article  CAS  PubMed  Google Scholar 

  3. Traveset A, Heleno R, Nogales M (2014) The ecology of seed dispersal. In: Gallagher RS (ed) Seeds: The Ecology of Regeneration in Plant Communities3rd edn. CABI, pp 62–93

  4. Jordano P (2017) What is long-distance dispersal? And a taxonomy of dispersal events. J Ecol 105:75–84. https://doi.org/10.1111/1365-2745.12690

    Article  Google Scholar 

  5. Pärtel M, Bennett JA, Zobel M (2016) Macroecology of biodiversity: disentangling local and regional effects. New Phytol 211:404–410. https://doi.org/10.1111/nph.13943

    Article  PubMed  Google Scholar 

  6. Zobel M (2016) The species pool concept as a framework for studying patterns of plant diversity. J Veg Sci 27:8–18. https://doi.org/10.1111/jvs.12333

    Article  Google Scholar 

  7. Ovaskainen O, Abrego N, Somervuo P, Palorinne I, Hardwick B, Pitkänen JM, Andrew NR, Niklaus PA, Schmidt NM, Seibold S, Vogt J, Zakharov EV, PDN H, Roslin T, Ivanova NV (2020) Monitoring fungal communities with the Global Spore Sampling Project. Front Ecol Evol 7:511. https://doi.org/10.3389/fevo.2019.00511

    Article  Google Scholar 

  8. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis3rd edn. Academic Press, London, p 800

    Google Scholar 

  9. Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115. https://doi.org/10.1111/nph.14976

    Article  PubMed  Google Scholar 

  10. van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423. https://doi.org/10.1111/nph.1328

    Article  PubMed  Google Scholar 

  11. Bardgett RD, van der Putten W (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511. https://doi.org/10.1038/nature13855

    Article  CAS  PubMed  Google Scholar 

  12. Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 16:1–13. https://doi.org/10.3389/fmicb.2015.01559

    Article  Google Scholar 

  13. Basu S, Rabara RC, Negi S (2018) AMF: the future prospect for sustainable agriculture. Physiol Mol Plant Pathol 102:36–45. https://doi.org/10.1016/j.pmpp.2017.11.007

    Article  Google Scholar 

  14. Bender SF, Wagg C, van der Heijden MGA (2016) An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol Evol 31:440–452. https://doi.org/10.1016/j.tree.2016.02.016

    Article  PubMed  Google Scholar 

  15. 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

    Article  CAS  Google Scholar 

  16. Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Ba A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Ndiaye C, Pärtel M, Reier U, Saks U, Singh R, Vasar M, Zobel M (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973. https://doi.org/10.1126/science.aab1161

    Article  CAS  PubMed  Google Scholar 

  17. Stürmer SL, Bever JD, Morton JB (2018) Biogeography of arbuscular mycorrhizal fungi (Glomeromycota): a phylogenetic perspective on species distribution patterns. Mycorrhiza 28:587–603. https://doi.org/10.1007/s00572-018-0864-6

    Article  PubMed  Google Scholar 

  18. Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921. https://doi.org/10.1126/science.289.5486.1920

    Article  CAS  PubMed  Google Scholar 

  19. Martin FM, Uroz S, Barker DG (2017) Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science 356:eaad4501. https://doi.org/10.1126/science.aad4501

    Article  CAS  PubMed  Google Scholar 

  20. Strullu-Derrien C, Selosse MA, Kenrick P, Martin FM (2018) The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics. New Phytol 220:1012–1030. https://doi.org/10.1111/nph.15076

    Article  PubMed  Google Scholar 

  21. Kivlin SN, Winston GC, Goulden ML, Treseder KK (2014) Environmental filtering affects soil fungal community composition more than dispersal limitations at regional scales. Fungal Ecol 12:14–25. https://doi.org/10.1016/j.funeco.2014.04.004

    Article  Google Scholar 

  22. García de León D, Moora M, Öpik M, Neuenkamp L, Gerz M, Jairus T, Vasar M, Bueno CG, Davison J, Zobel M (2016) Symbiont dynamics during ecosystem succession: co-occurring plant and arbuscular mycorrhizal fungal communities. FEMS Microbiol Ecol 92:fiw097. https://doi.org/10.1093/femsec/fiw097

    Article  CAS  PubMed  Google Scholar 

  23. Davison J, Moora M, Öpik M, Ainsaar L, Ducousso M, Hiiesalu I, Jairus T, Johnson N, Jourand P, Kalamees R, Koorem K, Meyer JY, Püssa K, Reier Ü, Pärtel M, Semchenko M, Traveset A, Vasar M, Zobel M (2018) Microbial island biogeography: isolation shapes the life history characteristics but not diversity of root-symbiotic fungal communities. ISME J 12:2211–2224. https://doi.org/10.1038/s41396-018-0196-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063. https://doi.org/10.1126/science.1070710

    Article  CAS  PubMed  Google Scholar 

  25. Bueno CG, Moora M (2019) How do arbuscular mycorrhizal fungi travel? New Phytol 222:1054–1060. https://doi.org/10.1111/nph.15722

    Article  Google Scholar 

  26. Allen MF, Hipps LE, Wooldridge GL (1989) Wind dispersal and subsequent establishment of VA mycorrhizal fungi across a successional arid landscape. Landsc Ecol 2:165–171. https://doi.org/10.1007/BF00126016

    Article  Google Scholar 

  27. Seres A, Bakonyi G, Posta K (2007) Collembola (Insecta) disperse the arbuscular mycorrhizal fungi in the soil: pot experiment. Pol J Ecol 55:395–399

    Google Scholar 

  28. 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

    Article  PubMed  Google Scholar 

  29. Egan C, Li DW, Klironomos J (2014) Detection of arbuscular mycorrhizal fungal spores in the air across different biomes and ecoregions. Fungal Ecol 12:26.31–26.31. https://doi.org/10.1016/j.funeco.2014.06.004

    Article  Google Scholar 

  30. LeBrun ES, Taylor DL, King RS, Back JA, Kang S (2018) Rivers may constitute an overlooked avenue of dispersal for terrestrial fungi. Fungal Ecol 32:72–79. https://doi.org/10.1016/j.funeco.2017.12.003

    Article  Google Scholar 

  31. Vašutova M, Mleczko P, López-García A, Maček I, Boros G, Ševčík J, Fujii S, Hackenberger D, Tuf IH, Hornung E, Páll-Gergely B, Kjøller R (2019) Taxi drivers: the role of animals in transporting mycorrhizal fungi. Mycorrhiza 29:413–434. https://doi.org/10.1007/s00572-019-00906-1

    Article  PubMed  Google Scholar 

  32. Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21:4122–4136. https://doi.org/10.1111/j.1365-294X.2012.05666.x

    Article  PubMed  Google Scholar 

  33. Dam N (2013) Spores do travel. Mycologia 105:1618–1622 10.3852–13035

    Article  Google Scholar 

  34. Reddell P, Spain A (1991) Earthworms as vectors of viable propagules of mycorrhizal fungi. Soil Biol Biochem 23:767–774. https://doi.org/10.1016/0038-0717(91)90147-C

    Article  Google Scholar 

  35. Janos DP, Sahley CT, Emmons LH (1995) Rodent dispersal of vesicular-arbuscular mycorrhizal fungi in Amazonian Peru. Ecology 76:1852–1858. https://doi.org/10.2307/1940717

    Article  Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. Olsson PA, Johansen A (2000) Lipid and fatty acid composition of hyphae and spores of arbuscular mycorrhizal fungi at different growth stages. Mycol Res 104:429–434. https://doi.org/10.1017/S0953756299001410

    Article  CAS  Google Scholar 

  38. Lekberg Y, Meadow J, Rohr JR, Redecker D, Zabinski CA (2011) Importance of dispersal and thermal environment for mycorrhizal communities: lessons from Yellowstone National Park. Ecology 92:1292–1302. https://doi.org/10.2307/23035000

    Article  PubMed  Google Scholar 

  39. Golan JJ, Pringle A (2017) Long-distance dispersal of fungi. Microb Spectr 5:1–24. https://doi.org/10.1128/microbiolspec.FUNK-0047-2016

    Article  Google Scholar 

  40. Aguilar-Trigueros CA, Hempel S, Powell JR, Cornwell WK, Rillig MC (2019) Bridging reproductive and microbial ecology: a case study in arbuscular mycorrhizal fungi. ISME J 13:873–884. https://doi.org/10.1038/s41396-018-0314-7

    Article  PubMed  Google Scholar 

  41. Novais CB, Sbrana C, Saggin Jr OJ, Siqueira JO, Giovannetti M (2013) Vegetative compatibility and anastomosis formation within and among individual germlings of tropical isolates of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:325–331. https://doi.org/10.1007/s00572-013-0478-y

    Article  CAS  PubMed  Google Scholar 

  42. Chagnon PL, Bradley RL, Maheral H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491. https://doi.org/10.1016/j.tplants.2013.05.001

    Article  CAS  PubMed  Google Scholar 

  43. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  44. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/

  45. Whitaker JO (1962) Endogone, Hymenogaster, and Melanogaster as small mammal foods. Am Midl Nat 67:152–156

    Article  Google Scholar 

  46. McIlveen WD, Cole Jr H (1976) Spore dispersal of Endogonaceae by worms, ants, wasps, and birds. Can J Bot 54:1486–1489. https://doi.org/10.1139/b76-161

    Article  Google Scholar 

  47. Trappe JM, Maser C (1976) Germination of spores of Glomus macrocarpus (Endogonaceae) after passage through a rodent digestive tract. Mycologia 68:433–436. https://doi.org/10.1080/00275514.1976.12019927

    Article  Google Scholar 

  48. Maser C, Trappe JM, Nussbaum RA (1978) Fungal-small mammal interrelationships with emphasis on Oregon coniferous forests. Ecology 59:799–809. https://doi.org/10.2307/1938784

    Article  Google Scholar 

  49. Rabatin SC, Stinner BR (1985) Arthropods as consumers of vesicular-arbuscular mycorrhizal fungi. Mycologia 77:320–322. https://doi.org/10.1080/00275514.1985.12025103

    Article  Google Scholar 

  50. Warner NJ, Allen MF, MacMahon JA (1987) Dispersal agents of vesicular-arbuscular mycorrhizal fungi in a disturbed arid ecosystem. Mycologia 79:721–730. https://doi.org/10.1080/00275514.1987.12025452

    Article  Google Scholar 

  51. Maser C, Maser Z, Molina R (1988) Small-mammal mycophagy in rangelands of central and Southeastern Oregon. J Range Manag 41:309–312. https://doi.org/10.2307/3899385

    Article  Google Scholar 

  52. Blaschke H, Bäumler W (1989) Mycophagy and spore dispersal by small mammals in Bavarian forests. For Ecol Manag 26:237–245. https://doi.org/10.1016/0378-1127(89)90084-4

    Article  Google Scholar 

  53. Perez-Calvo JG, Maser Z, Maser C (1989) Note on fungi in small mammals from the Nothofagus forest in Argentina. Gr Bas Nat 49:618–620 https://scholarsarchive.byu.edu/gbn/vol49/iss4/18

    Google Scholar 

  54. 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. https://doi.org/10.1002/j.1537-2197.1990.tb13577.x

    Article  CAS  PubMed  Google Scholar 

  55. 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

    Article  Google Scholar 

  56. McGee PA, Pattinson GS, Heath RA, Newman CA, Allen SJ (1997) Survival of propagules of arbuscular mycorrhizal fungi in soils in eastern Australia used to grow cotton. New Phytol 135:773–780. https://doi.org/10.1046/j.1469-8137.1997.00709.x

    Article  Google Scholar 

  57. Pattinson GS, Smith SE, Doube BM (1997) Earthworm Aporrectodea trapezoides had no effect on the dispersal of vesicular-arbuscular mycorrhizal fungi, Glomus intraradices. Soil Biol Biochem 29:1079–1088. https://doi.org/10.1016/S0038-0717(97)00005-9

    Article  CAS  Google Scholar 

  58. Reddell P, Spain AV, Hopkins M (1997) Dispersal of spores of mycorrhizal fungi in scats of native mammals in tropical forests in Northeastern Australia. Biotropica 29:184–192. https://doi.org/10.1111/j.1744-7429.1997.tb00023.x

    Article  Google Scholar 

  59. Mangan SA, Adler GH (1999) Consumption of arbuscular mycorrhizal fungi by spiny rats (Proechimys semispinosus) in eight isolated populations. J Trop Ecol 15:779–790. https://doi.org/10.1017/S0266467499001170

    Article  Google Scholar 

  60. 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. https://doi.org/10.1644/1545-1542(2000)081<0563:COAMFB>2.0.CO;2

    Article  Google Scholar 

  61. Vernes K, Castellano M, Johnson CN (2001) Effects of season and fire on the diversity of hypogeous fungi consumed by a tropical mycophagous marsupial. J Anim Ecol 70:945–954. https://doi.org/10.1046/j.0021-8790.2001.00564.x

    Article  Google Scholar 

  62. Renker C, Otto P, Schneider K, Zimdars B, Maraun M, Buscot F (2005) Oribatid mites as potential vectors for soil microfungi: study of mite-associated fungal species. Microb Ecol 50:518–528. https://doi.org/10.1007/s00248-005-5017-8

    Article  CAS  PubMed  Google Scholar 

  63. Jacobs KM, Luoma DL (2008) Small mammal mycophagy response to variations in green-tree retention. J Wildl Manag 72:1747–1755. https://doi.org/10.2193/2007-341

    Article  Google Scholar 

  64. Harner MJ, Piotrowski JS, Lekberg Y, Stanford JA, Rillig M (2009) Heterogeneity in mycorrhizal inoculum potential of flood-deposited sediments. Aquat Sci 71:331–337. https://doi.org/10.1007/s00027-009-9198-y

    Article  CAS  Google Scholar 

  65. Fracchia S, Krapovickas L, Aranda-Rickert A, Valentinuzzi VS (2011) Dispersal of arbuscular mycorrhizal fungi and dark septate endophytes by Ctenomys cf. knighti (Rodentia) in the northern Monte Desert of Argentina. J Arid Environ 75:1016–1023. https://doi.org/10.1016/j.jaridenv.2011.04.034

    Article  Google Scholar 

  66. Katarzyte M, Kutorga E (2011) Small mammal mycophagy in hemiboreal forest communities of Lithuania. Cent Eur J Biol 6:446–456. https://doi.org/10.2478/s11535-011-0006-z

    Article  Google Scholar 

  67. Ambarish CN, Sridhar KR (2014) Do the giant pill-millipedes (Arthrosphaera: Sphaerotheriida) disseminate arbuscular mycorrhizal spores in the Western Ghats? Symbiosis 64:95–99. https://doi.org/10.1007/s13199-014-0306-y

    Article  Google Scholar 

  68. Sahley CT, Cervantes K, Pacheco V, Salas E, Paredes D, Alonso A (2015) Diet of sigmodontine rodent assemblage in a Peruvian montane forest. J Mammal 96:1071–1080. https://doi.org/10.1093/jmammal/gyv112

    Article  PubMed  PubMed Central  Google Scholar 

  69. 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. https://doi.org/10.1656/045.022.0123

    Article  Google Scholar 

  70. Nielsen KB, Kjoller 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

    Article  Google Scholar 

  71. Adler GH, Counsell E, Seamon JO, Bentivenga SP (2017) Exotic rats consume sporocarps of arbuscular mycorrhizal fungi in American Samoa. Mammalia 82:1–4. https://doi.org/10.1515/mammalia-2016-0135

    Article  Google Scholar 

  72. Correia M, Heleno R, da Silva LP, Costa JM, Rodríguez-Echeverría S (2019) First evidence for the joint dispersal of mycorrhizal fungi and plant diaspores by birds. New Phytol 222:1054–1060. https://doi.org/10.1111/nph.15571

    Article  PubMed  Google Scholar 

  73. Chaudhary VB, Nolimal S, Sosa-Hernández MA, Egan C, Kastens J (2020) Trait-based aerial dispersal of arbuscular mycorrhizal fungi. New Phytol Accepted Manuscript. https://doi.org/10.1111/nph.16667

  74. Norros V, Rannik Ü, Hussein T, Petäjä T, Vesala T, Ovaskainen O (2014) Do small spores disperse further than large spores? Ecology 95:1612–1621. https://doi.org/10.1890/13-0877.1

    Article  PubMed  Google Scholar 

  75. Varela-Cervero S, López-García A, Barea JM, Azcón-Aguilar C (2016) Differences in the composition of arbuscular mycorrhizal fungal communities promoted by different propagule forms from a Mediterranean shrubland. Mycorrhiza 26:489–496. https://doi.org/10.1007/s00572-016-0687-2

    Article  PubMed  Google Scholar 

  76. Öpik M, Davison J (2016) Uniting species- and community-oriented approaches to understand arbuscular mycorrhizal fungal diversity. Fungal Ecol 24:106–113. https://doi.org/10.1016/j.funeco.2016.07.005

    Article  Google Scholar 

  77. Camargo-Ricalde SL (2002) Dispersal, distribution and establishment of arbuscular mycorrhizal fungi: a review. Bol Soc Bot Méx 71:33–44

    Google Scholar 

  78. Bielčik M, Aguilar-Trigueros CA, Lakovic M, Jeltsch F, Rillig MC (2019) The role of active movement in fungal ecology and community assembly. Mov Ecol 7:36. https://doi.org/10.1186/s40462-019-0180-6

    Article  PubMed  PubMed Central  Google Scholar 

  79. Ianson DC, Allen MF (1986) The effects of soil mixture on extraction of vesicular-arbuscular mycorrhizal fungal spores from arid sites. Mycologia 78:164–168. https://doi.org/10.1080/00275514.1986.12025227

    Article  Google Scholar 

  80. Tommerup IC (1983) Spore dormancy in vesicular-arbuscular mycorrhizal fungi. Trans Br Mycol Soc 81:37–45. https://doi.org/10.1016/S0007-1536(83)80201-0

    Article  Google Scholar 

  81. Juge C, Samson J, Bastien C, Vierheilig H, Coughlan A, Piché Y (2002) Breaking dormancy in spores of the arbuscular mycorrhizal fungus Glomus intraradices: a critical cold-storage period. Mycorrhiza 12:37–42. https://doi.org/10.1007/s00572-0151-8

    Article  PubMed  Google Scholar 

  82. Traveset A, Verdú M (2002) A meta-analysis of the effect of gut treatment on seed germination. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and Frugivory: Ecology, Evolution and Conservation, 2nd edn. CABI Publishing, Wallingford, pp 339–350

  83. Treseder KK, Allen EB, Egerton-Warburton LM, Hart M, Klironmos JN, Maherali H, Tedersoo L (2018) Arbuscular mycorrhizal fungi as mediators of ecosystem responses to nitrogen deposition: a trait-based predictive framework. J Ecol 106:480–489. https://doi.org/10.1111/1365-2745.12919

    Article  CAS  Google Scholar 

  84. Forbes ES, Cushmanb JH, Burkepilea DE, Young TP, Klopea M, Young HS (2019) Synthesizing the effects of large, wild herbivore exclusion on ecosystem function. Funct Ecol 33:1597–1610. https://doi.org/10.5061/dryad.3tf4mt4

    Article  Google Scholar 

  85. Fleming PA, Anderson H, Prendergast A, Bretz MR, Valentine LE, Hardy GESSJ (2017) Is the loss of Australian digging mammals contributing to a deterioration in ecosystem function? Mammal Rev 44:94–108. https://doi.org/10.1111/mam.12014

    Article  Google Scholar 

  86. Coggan NV, Hayward MW, Gibb H (2018) A global database and “state of the field” review of research into ecosystem engineering by land mammals. J Anim Ecol 87:974–994. https://doi.org/10.1111/1365-2656.12819

    Article  PubMed  Google Scholar 

  87. Cadotte MW (2006) Dispersal and species diversity: a meta-analysis. Am Nat 167:913–924. https://doi.org/10.1086/504850

    Article  PubMed  Google Scholar 

  88. Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51. https://doi.org/10.1086/418432

    Article  Google Scholar 

  89. Gehring CA, Wolf JE, Theimer TC (2002) Terrestrial vertebrates promote arbuscular mycorrhizal fungal diversity and inoculum potential in a rain forest soil. Ecol Lett 5:540–548. https://doi.org/10.1046/j.1461-0248.2002.00353.x

    Article  Google Scholar 

  90. Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B (2014) Defaunation in the Anthropocene. Science 345:401–406. https://doi.org/10.1126/science.1251817

    Article  CAS  PubMed  Google Scholar 

  91. Soteras F, Ibarra C, Geml J, Barrios-García MN, Domínguez LS, Nouhra ER (2017) Mycophagy by invasive wild boar (Sus scrofa) facilitates dispersal of native and introduced mycorrhizal fungi in Patagonia, Argentina. Fungal Ecol 26:51–58. https://doi.org/10.1016/j.funeco.2016.11.008

    Article  Google Scholar 

  92. Savary R, Masclaux FG, Wyss T, Droh G, Corella JC, Machado AP, Morton JB, Sanders IR (2018) A population genomics approach shows widespread geographical distribution of cryptic genomic forms of the symbiotic fungus Rhizophagus irregularis. ISME J 12:17–30. https://doi.org/10.1038/ismej.2017.153

    Article  PubMed  Google Scholar 

  93. Hart MM, Aleklett K, Chagnon PL, Egan C, Ghignone S, Helgason T, Lekberg Y, Öpik M, Pickles BJ, Waller L (2015) Navigating the labyrinth: a guide to sequence-based community ecology of arbuscular mycorrhizal fungi. New Phytol 207:235–247. https://doi.org/10.1111/nph.13340

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank John Davison and the three anonymous referees for valuable comments on an earlier version of this manuscript.

Funding

This research was funded by São Paulo Research Foundation (FAPESP) processes 2016/25197-0, 2018/16697-4 (granted to CP) and 2018/00212-1 (granted to LB). MG received a fellowship from the National Council for Scientific and Technological Development CNPq. MÖ and CGB are funded by the European Regional Development Fund (Centre of Excellence EcolChange).

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All authors contributed to this review paper. Claudia Paz had the idea for the article; performed the literature search, data preparation, analyses and figures; and wrote the first draft. Maarja Öpik and C. Guillermo Bueno critically revised the work and contributed to writing and editing; Leticia Bulascoschi performed literature search and database organization; and Mauro Galetti contributed to article conception, critical revision and editing of drafts. All authors read and approved the final version of the manuscript.

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Correspondence to Claudia Paz.

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Paz, C., Öpik, M., Bulascoschi, L. et al. Dispersal of Arbuscular Mycorrhizal Fungi: Evidence and Insights for Ecological Studies. Microb Ecol 81, 283–292 (2021). https://doi.org/10.1007/s00248-020-01582-x

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  • DOI: https://doi.org/10.1007/s00248-020-01582-x

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