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Mycorrhizal Studies in Temperate Rainforests of Southern Chile

  • Roberto GodoyEmail author
  • César Marín
Chapter
Part of the Fungal Biology book series (FUNGBIO)

Abstract

Old-growth temperate rainforests, located at the Patagonian and Valdivian regions of southern Chile and Argentina, represent unique ecosystems in South America. These forests are characterized by a large amount of precipitation, with very little to none atmospheric pollution, and a flora derived from Gondwanian elements. The mycorrhizal traits of the dominant plants of these ecosystems are also exceptional: the angiosperm Nothofagus spp. associates with ectomycorrhizal (EM) fungi, while the native conifer species associate with arbuscular mycorrhizal (AM) fungi, an opposite pattern to that of the Northern hemisphere. On this chapter we present an overview of the mycorrhizal types of 245 vascular plant species, where 187 species associate with AM fungi, seven with EM fungi, 14 with other mycorrhizal types, and 37 plant species are non-mycorrhizal. On these southern Chile ecosystems, we also show the role of mycorrhizal fungi on crucial ecosystem processes, as biogenic weathering, and their potential use as ecological restoration tools for the re-establishment of native flora. Specifically, we found that the co-inoculation of two EM fungi species significantly increases the growth of Nothofagus spp. as compared to singular inoculations. On these temperate rainforests, mycorrhizal fungi play key roles on nutrient cycling, maintenance of biodiversity, and ecosystem productivity.

Keywords

Biogenic weathering Conifers Ecological restoration Nothofagus spp. Old-growth forest 

Notes

Acknowledgments

R.G and C.M. were funded by the project Fondecyt 1190642. C.M. was funded by the Universidad de O’Higgins post-doctoral research fund. Special thanks to Dr. Jens Boy for support in the laboratory at the Institute of Soil Science, Leibniz Universität Hannover, Germany.

References

  1. Aguilera-Betti I, Muñoz AA, Stahle D, Figueroa G, Duarte F, González-Reyes Á, Christie D, Lara A, González ME, Sheppard PR, Sauchyn AM, Toledo-Guerrero I, Olea M, Apaz P, Fernandez A (2017) The First Millennium-Age Araucaria araucana in Patagonia. Tree-Ring Res 73(1):53–56CrossRefGoogle Scholar
  2. Aguilera P, Marín C, Oehl F, Godoy R, Borie F, Cornejo PE (2017) Selection of aluminum tolerant cereal genotypes strongly influences the arbuscular mycorrhizal fungal communities in an acidic Andosol. Agric Ecosyst Environ 246:86–93CrossRefGoogle Scholar
  3. Amano T, Sutherland WJ (2013) Four barriers to the global understanding of biodiversity conservation: wealth, language, geographical location and security. Proc R Soc B 280(1756):20122649.  https://doi.org/10.1098/rspb.2012.2649 CrossRefGoogle Scholar
  4. Armesto JJ, Manuschevich D, Mora A, Smith-Ramírez C, Rozzi R, Abarzúa AM, Marquet PA (2010) From the Holocene to the Anthropocene: A historical framework for land cover change in southwestern South America in the past 15,000 years. Land Use Policy 27(2):148–160CrossRefGoogle Scholar
  5. Armesto JJ, Smith-Ramírez C, Carmona MR, Celis-Diez JL, Díaz IA, Gaxiola A, Gutiérrez AG, Núñez-Avila MC, Pérez CA, Rozzi R (2009) Old-growth temperate rainforests of South America: conservation, plant–animal interactions, and baseline biogeochemical processes. In: Wirth C, Gleixner G, Heimann M (eds) Old-growth forests. Springer Berlin Heidelberg, Berlin, p 367–390CrossRefGoogle Scholar
  6. Banfield JF, Barker WW, Welch SA, Taunton A (1999) Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. P Nat Acad Sci USA 96(7):3404–3411CrossRefGoogle Scholar
  7. Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515(7528):505–511CrossRefGoogle Scholar
  8. Bekessy S, Allnutt T, Premoli A, Lara A, Ennos R, Burgman M, Cortes M, Newton AC (2002) Genetic variation in the vulnerable and endemic Monkey Puzzle tree, detected using RAPDs. Heredity 88:243–249PubMedCrossRefGoogle Scholar
  9. Bekessy S, Lara A, González M, Cortés M, Premoli A, Newton A (2004) Variación en Araucaria araucana (Molina) K. Koch (Araucaria o Pehuén). In: Donoso C, Premoli A, Gallo L, Ipinza R (eds) Variación Intraespecífica en las especies arbóreas de los bosques templados de Chile y Argentina. Editorial Universitaria, Santiago, p. 215–232Google Scholar
  10. Berner RA (1992) Weathering, plants, and the long-term carbon cycle. Geochim Cosmochim Acta 56(8):3225–3231CrossRefGoogle Scholar
  11. Bowman DM, Moreira-Muñoz A, Kolden CA, Chávez RO, Muñoz AA, Salinas F, González-Reyes A, Rocco R, de la Barrera F, Williamson GJ, Borchers N, Cifuentes LA, Abatzoglou JT, Johnston FH (2018) Human–environmental drivers and impacts of the globally extreme 2017 Chilean fires. Ambio 48(4):350–362PubMedCrossRefGoogle Scholar
  12. Boy J, Wilcke W (2008) Tropical Andean forest derives calcium and magnesium from Saharan dust. Global Biogeochem Cycles 22(1):GB1027CrossRefGoogle Scholar
  13. Boy J, Godoy R, Guevara G (2014) Transporte de aerosoles, biometeorización y cambio global. In: Donoso C, González M, Lara A (eds) Ecología Forestal: Bases para el Manejo Sustentable y Conservación de los Bosques Nativos de Chile. Ediciones Universidad Austral de Chile, Valdivia, p. 281–295.Google Scholar
  14. Boy J, Rollenbeck R, Valarezo C, Wilcke W (2008) Amazonian biomass burning-derived acid and nutrient deposition in the north Andean montane forest of Ecuador. Global Biogeochemical Cycles 22(4):GB4011CrossRefGoogle Scholar
  15. Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220(4):1108–1115CrossRefGoogle Scholar
  16. Bueno CG, Marín C, Silva-Flores P, Aguilera P, Godoy R (2017) Think globally, research locally: contrasting patterns of mycorrhizal symbiosis in South America. New Phytol 215(4):1306–1309CrossRefGoogle Scholar
  17. Burford EP, Fomina M, Gadd GM (2003) Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineral Mag 67(6):1127–1155CrossRefGoogle Scholar
  18. Carrillo R, Godoy R, Peredo H (1992) Simbiosis micorrícica en comunidades boscosas del Valle Central en el sur de Chile. Bosque 13(2):57–67CrossRefGoogle Scholar
  19. Carú M (1993) Characterization of native Frankia strains isolated from Chilean shrubs (Rhamnaceae). Plant Soil 157(1):137–145Google Scholar
  20. Castillo C-G, Borie F, Godoy R, Rubio R, Sieverding E (2006) Diversity of mycorrhizal plant species and arbuscular mycorrhizal fungi in evergreen forest, deciduous forest and grassland ecosystems of Southern Chile. J Appl Bot Food Qual 80(1):40–47Google Scholar
  21. Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD (2015) Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol 205(4):1525–1536PubMedCrossRefGoogle Scholar
  22. Cortés M (2016) Restauración ecológica de los bosques de Araucaria araucana (Molina) K. Koch de la Cordillera de Nahuelbuta en la región de la Araucanía, Chile. Doctoral thesis, Universidad Austral de Chile.Google Scholar
  23. Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Ndiaye C, Pärtel M, Reier Ü, Saks Ü, Singh R, Vasar M, Zobel M (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349(6251):970–973PubMedPubMedCentralCrossRefGoogle Scholar
  24. Etcheverría P, Huygens D, Godoy R, Borie F, Boeckx P (2009) Arbuscular mycorrhizal fungi contribute to 13C and 15N enrichment of soil organic matter in forest soils. Soil Biol Biochem 41(4):858–861CrossRefGoogle Scholar
  25. Fernández N, Fontenla S, Messuti MI (2005). Micorrizas en pteridofitas de los bosques templado-lluviosos del Noroeste de Patagonia. II Convención Ambiental Universitaria Patagónica, Universidad Nacional del Comahue, Bariloche, Argentina.Google Scholar
  26. Finlay R, Wallander H, Smits M, Holmstrom S, van Hees P, Lian B, Rosling A (2009) The role of fungi in biogenic weathering in boreal forest soils. Fungal Biol Rev 23(4):101–106CrossRefGoogle Scholar
  27. Flores R, Godoy R, Palfner G (1997) Morfo-anatomía de la ectomicorriza Cenococcum geophilum Fr. en Nothofagus alessandrii Esp. Gayana Bot 54(2):157–162Google Scholar
  28. Fontenla S, Godoy R, Rosso P, Havrylenko M (1998) Root associations in Austrocedrus forests and seasonal dynamics of arbuscular mycorrhizas. Mycorrhiza 8(1):29–33CrossRefGoogle Scholar
  29. Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111(1):3–49PubMedCrossRefGoogle Scholar
  30. Garrido N (1988) Agaricales s. l. und ihre mykorrhizen in den Nothofagus-Wäldern mittelchiles. Bibliotheca Mycologica 120. J., Cramer, Berlin.Google Scholar
  31. Godoy R, Carrillo R, Peredo H (1995) Ökologische und experimentelle Arbeiten über Mykorrhiza in Naturwäldern Südchiles. Ver. Ges Ökol 24:619–622.Google Scholar
  32. Godoy R, Valenzuela E, Guevara G, Boy J, Barrientos M, Matus F (2014) Biogeoquímica en bosques templados del sur de Chile. In: Donoso C, González ME, Lara A (eds) Ecología Forestal. Editorial Universidad Austral de Chile, Valdivia, p. 257–280Google Scholar
  33. Godoy R, Mayr R (1989) Caracterización morfológica de micorrizas vesículo-arbusculares en coníferas endémicas del sur de Chile. Bosque 10(2):89–98CrossRefGoogle Scholar
  34. Godoy R, Oyarzún C (1998) Water chemistry in forests of southern Chile. Ver Ges Ökol 28:471–474Google Scholar
  35. Godoy R, Oyarzún C, Bahamones J (1999) Flujos hidroquímicos en un bosque de Nothofagus pumilio en el Parque Nacional Puyehue, sur de Chile. Rev Chil Hist Nat 72:579–594Google Scholar
  36. Godoy R, Oyarzún C, Gerding V (2001) Precipitation chemistry in deciduous and evergreen Nothofagus forests of southern Chile under a low-deposition climate. Basic Appl Ecol 2(1):65–72CrossRefGoogle Scholar
  37. Godoy R, Paulino L, Oyarzún C, Boeckx P (2003) Atmospheric N deposition in Central and Southern Chile, an overview. Gayana Bot 60(1):47–53CrossRefGoogle Scholar
  38. Godoy R, Paulino L, Valenzuela E, Oyarzún C, Huygens D, Boeckx P (2009) Temperate ecosystems of Chile: characteristic biogeochemical cycles and disturbance regimes. In: Oyarzún C, Verhoest N, Boeckx P, Godoy R (eds) Ecological advances on Chilean temperate forests. Academia Press, Gehnt, p. 31–40Google Scholar
  39. Godoy R, Palfner G (1997) Ectomicorrizas en Nothofagus alpina (P. et E.) Oerst y N. dombeyi (Mirb.) Oerst. del Sur de Chile. Bol Micol 12:55–61Google Scholar
  40. Godoy R, Romero R, Carrillo R (1994) Estatus micotrófico de la flora vascular en bosques de coníferas nativas. Rev Chil Hist Nat 67:209–220Google Scholar
  41. Hedin LO, Hetherington ED (1996) Atmospheric and geologic constraints on the biogeochemistry of North and South American temperate rainforests. In: Lawford RG, Alaback P, Fuentes E (eds) High-Latitude Rainforests and Associated Ecosystems of the West Coast of the Americas. Springer, New York, p. 55–74CrossRefGoogle Scholar
  42. Hoffland E, Kuyper TW, Wallander H, Plassard C, Gorbushina AA, Haselwandter K, Holmström S, Landeweert R, Lundström US, Rosling A, Sen R, Smits MM, van Hees PAW, van Breemen N (2004). The role of fungi in weathering. Front Ecol Environ 2(5):258–264CrossRefGoogle Scholar
  43. Kennedy MJ, Hedin LO, Derry LA (2002) Decoupling of unpolluted temperate forests from rock nutrient sources revealed by natural 87Sr/86Sr and 84Sr tracer addition. P Nat Acad Sci USA 99(15):9639–9644CrossRefGoogle Scholar
  44. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92(4):486–488CrossRefGoogle Scholar
  45. Lara A, Little C, Cortés M, Cruz E, González ME, Echeverría C, Suárez J, Bahamondez A, Coopman R (2014) Restauración de ecosistemas forestales. In: Donoso C, González ME, Lara A (eds) Ecología Forestal. Editorial Universidad Austral de Chile, Valdivia, p.605–672Google Scholar
  46. Lara A, Villalba R (1993) A 3620-year temperature record from Fitzroya cupressoides tree rings in southern South America. Science 260(5111):1104–1106PubMedCrossRefGoogle Scholar
  47. Marín C (2018a) Fungal biodiversity associated to bioweathering processes in a chronosequence of temperate rainforests in southern Chile. Doctoral Thesis, Universidad Austral de Chile.Google Scholar
  48. Marín C, Aguilera P, Cornejo P, Godoy R, Oehl F, Palfner G, Boy J (2016) Arbuscular mycorrhizal assemblages along contrasting Andean forests of Southern Chile. J Soil Sci Plant Nutr 16(4):916–929Google Scholar
  49. Marín C, Aguilera P, Oehl F, Godoy R (2017a) Factors affecting arbuscular mycorrhizal fungi of Chilean temperate rainforests. J Soil Sci Plant Nutr 17(4):966–984CrossRefGoogle Scholar
  50. Marín C, Godoy R, Valenzuela E, Schloter M, Wubet T, Boy J, Gschwendtner S (2017b) Functional land-use change effects on soil fungal communities in Chilean temperate rainforests. J Soil Sci Plant Nutr 17(4):985–1002CrossRefGoogle Scholar
  51. Marín C, Valenzuela E, Godoy R, Palfner G (2018a) Diversity and growth-effects of ectomycorrhizal fungi of a Nothofagus pumilio forest in the Andes of Southern Chile. Bol Micol 33(1):9–20CrossRefGoogle Scholar
  52. Marín C, Torres D, Furci G, Godoy R, Palfner G (2018b) Estado del arte de la conservación del reino Fungi en Chile. Biodiversidata 7:98–115Google Scholar
  53. Nouhra ER, Urcelay C, Longo MS, Fontenla S (2012) Differential hypogeous sporocarp production from Nothofagus dombeyi and N. pumilio forests in southern Argentina. Mycologia 104(1):45–52PubMedPubMedCentralCrossRefGoogle Scholar
  54. Nouhra E, Urcelay C, Longo S, Tedersoo L (2013) Ectomycorrhizal fungal communities associated to Nothofagus species in Northern Patagonia. Mycorrhiza 23(6):487–496CrossRefGoogle Scholar
  55. Oeser RA, Stroncik N, Moskwa LM, Bernhard N, Schaller M, Canessa R, van den Brink L, Köster M, Brucker E, Stock S, Fuentes JP, Godoy R, Matus FJ, Oses Pedraza R, Osses McIntyre P, Paulino L, Seguel O, Bader MY, Boy J, Dippold MA, Ehlers TA, Kühn P, Kuzyakov Y, Leinweber P, Scholten T, Spielvogel S, Spohn M, Übernickel K, Tielbörger K, Wagner D, von Blanckenburg F (2018) Chemistry and microbiology of the Critical Zone along a steep climate and vegetation gradient in the Chilean Coastal Cordillera. Catena 170:183–203CrossRefGoogle Scholar
  56. Oyarzún CE, Godoy R, Leiva S (2002) Depositación atmosférica de nitrógeno en un transecto Valle Longitudinal-Cordillera de los Andes, Centro-Sur de Chile. Rev Chil Hist Nat 75(1):165–175CrossRefGoogle Scholar
  57. Oyarzún CE, Godoy R, de Schrijver A, Staelens J, Lust N (2004) Water chemistry and nutrient budgets in an undisturbed evergreen rainforest of southern Chile. Biogeochemistry 71(1):107–123CrossRefGoogle Scholar
  58. Oyarzún CE, Godoy R, Staelens J, Donoso PJ, Verhoest NE (2011) Seasonal and annual throughfall and stemflow in Andean temperate rainforests. Hydrol Process 25(4):623–633CrossRefGoogle Scholar
  59. Oyarzún C, Aracena C, Rutherford P, Godoy R, de Schrijver A (2007) Effects of land use conversion from native forests to exotic plantations on nitrogen and phosphorus retention in catchments of southern Chile. Water Air Soil Pollut 179(1–4):341–350CrossRefGoogle Scholar
  60. Oyarzún C, Godoy R, Sepúlveda A (1998) Water and nutrient fluxes in a cool temperate rainforest at the Cordillera de la Costa in Southern Chile. Hydrol Process 12(7):1067–1077CrossRefGoogle Scholar
  61. Oyarzún C, Verhoest N, Boeckx P, Godoy R (2009) Ecological advances on Chilean temperate forests. Academia Press, Ghent.Google Scholar
  62. Palfner G (2001) Taxonomische studien an Ektomykorrhizen aus den Nothofagus-Waldern Mittelsudchiles. Bibliotheca Mycologica 190. J., Cramer, Berlin.Google Scholar
  63. Palfner G (2002) Diversity and community studies on Fagus/Nothofagus ectomicorrhizae from European and South American Forest. In: de Schrijver A, Kint V, Lust N (eds) Procceding of the Workshop Comparison of ecosystems functioning and biogeochemical cycles in temperate forests in Southern Chile and Flanders. Academia Press, Ghent, p. 119–129Google Scholar
  64. Palfner G, Godoy R (1996a) “Nothofagirhiza vinicolor” + Nothofagus pumilio (Poepp. et Endl.) Kraser. Descriptions of Ectomycorrhizae 1:65–70Google Scholar
  65. Palfner G, Godoy R (1996b) Russula fuegiana Singer + Nothofagus pumilio (Poepp. et Endl.) Krasser. Descriptions of Ectomycorrhizae 1:131–136Google Scholar
  66. Palfner G, Canseco MI, Casanova-Katny A (2008) Post-fire seedlings of Nothofagus alpina in Southern Chile show strong dominance of a single ectomycorrhizal fungus and a vertical shift in root architecture. Plant Soil 313(1–2):237–250CrossRefGoogle Scholar
  67. Paulino L, Godoy R, Boeckx P (2009) Ecosystem responses of Andean Araucaria-Nothofagus communities after a wildfire. In: Oyarzún C, Verhoest N, Boeckx P, Godoy R (eds) Ecological advances on Chilean temperate forests. Academia Press, Gehnt, p. 117–132Google Scholar
  68. Peay KG, Kennedy PG, Talbot JM (2016) Dimensions of biodiversity in the Earth mycobiome. Nat Rev Microbiol 14(7):434–447CrossRefGoogle Scholar
  69. Pereira G, Suz LM, Albornoz V, Romero C, Garcia L, Leiva V, Atala C (2018) Mycorrhizal fungi associated with Codonorchis lessonii (Brongn.) Lindl., a terrestrial orchid from Chile. Gayana Bot 75(1):447–458CrossRefGoogle Scholar
  70. Ritchie GA (1984) Assessing seedling quality. In: Duryea ML, Landis TD (eds) Forestry nursery manual: production of bareroot seedlings. Springer, The Hague, p. 243–259CrossRefGoogle Scholar
  71. Rivas Y, Canseco MI, Knicker H, Etcheverría P, Godoy R, Matus F, Valenzuela E, Gallardo R (2016) Variación en el contenido de glomalina relacionada a las proteínas del suelo, después de un incendio forestal en un Andisol en bosques de Araucaria araucana del centro-sur de Chile. Bosque 37,409–417Google Scholar
  72. Rivas Y, Huygens D, Knicker H, Godoy R, Matus F, Boeckx P (2012) Soil nitrogen dynamics three years after a severe Araucaria-Nothofagus forest fire. Austral Ecol 37:153–163CrossRefGoogle Scholar
  73. Rodriguez R, Marticorena C, Alarcón D, Baeza C, Cavieres L, Finot VL, Fuentes N, Kiessling A, Mihoc M, Pauchard A, Ruiz E, Sanchez P, Marticorena A (2018) Catálogo de las plantas vasculares de Chile. Gayana Bot 75(1):1–430CrossRefGoogle Scholar
  74. Rosling A, Lindahl BD, Finlay RD (2004) Carbon allocation to ectomycorrhizal roots and mycelium colonising different mineral substrates. New Phytol 162(3):795–802CrossRefGoogle Scholar
  75. Sadzawka A, Carrasco MA, Grez R, Mora ML, Flores H, Neaman A (2006) Métodos de análisis recomendados para los suelos de Chile. Revisión 2006. Serie Actas INIA 34. Google Scholar
  76. Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26(1):39–60CrossRefGoogle Scholar
  77. Singer R (1969) Mycoflora Australis. Beihefte Nova Hedwigia 29, J. Cramer, Lehre.Google Scholar
  78. Singer R (1970) Phaeocollybia (Cortinariaceae, Basidiomycetes). Flora Neotropica 4:1–13Google Scholar
  79. Singer R, Moser M, Gamundí I, Ellas R, Sarmiento G (1965) Forest mycology and forest communities in South America. Mycopath Mycol Appl 26(2–3):129–191CrossRefGoogle Scholar
  80. Singer R, Morello JH (1960) Ectotrophic forest tree mycorrhizae and forest communities. Ecology 41(3):549–551CrossRefGoogle Scholar
  81. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis (Third Edition). Academic Press, New York.CrossRefGoogle Scholar
  82. Smits MM, Wallander H (2017) Role of mycorrhizal symbiosis in mineral weathering and nutrient mining from soil parent material. In: Johnson N, Gehring C, Jansa J (eds) Mycorrhizal Mediation of Soil: Fertility, Structure, and Carbon Storage. Elsevier, New York, p. 35–46CrossRefGoogle Scholar
  83. Staelens J, de Schrijver A, Oyarzún C, Lust N (2003) Comparison of dry deposition and canopy exchange of base cations in temperate hardwood forests in Flanders and Chile. Gayana Bot 60(1):9–16Google Scholar
  84. Staelens J, Godoy R, Oyarzún C, Thibo K, Verheyen K (2005) Nitrogen fluxes in throughfall and litterfall in two Nothofagus forests in southern Chile. Gayana Bot 62(2):63–71Google Scholar
  85. Staelens J, Oyarzún C, Almonacid L, Padila E, Verheyen (2009) Aboveground nutrient cycling in temperate forest ecosystems of southern Chile. In: Oyarzún C, Verhoest N, Boeckx P, Godoy R (eds) Ecological advances on Chilean temperate forests. Academia Press, Gehnt, p. 103–106Google Scholar
  86. Taylor LL, Leake JR, Quirk J, Hardy K, Banwart SA, Beerling DJ (2009) Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm. Geobiology 7(2):171–191PubMedCrossRefGoogle Scholar
  87. Tedersoo L (2017) Biogeography of mycorrhizal symbiosis. Springer, New York.Google Scholar
  88. Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, Ruiz L. V, Vasco-Palacios AM, Thu PQ, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch K, Põldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Pärtel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson RH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson K-H, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo L, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk, Drenkhan R, Dearnaley J, De Kesel A, Dang T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K (2014) Global diversity and geography of soil fungi. Science 346(6213):1256688CrossRefGoogle Scholar
  89. Thomas E, Jalonen R, Loo J, Boshier D, Gallo L, Cavers S, Bordács S, Smith P, Bozzano M (2014) Genetic considerations in ecosystem restoration using native tree species. Forest Ecol Manag 333:66–75CrossRefGoogle Scholar
  90. Trierveiler-Pereira L, Smith ME, Trappe JM, Nouhra ER (2015) Sequestrate fungi from Patagonian Nothofagus forests: Cystangium (Russulaceae, Basidiomycota). Mycologia 107(1):90–103PubMedPubMedCentralCrossRefGoogle Scholar
  91. Tripp EA, Zhang N, Schneider H, Huang Y, Mueller GM, Hu Z, Häggblom M, Bhattacharya D (2017) Reshaping Darwin’s Tree: Impact of the Symbiome. Trends Ecol Evol 32(8):552–555CrossRefGoogle Scholar
  92. Truong C, Mujic AB, Healy R, Kuhar F, Furci G, Torres D, Niskanen T, Sandoval-Leiva PA, Fernández N, Escobar JM, Moretto A, Palfner G, Pfister D, Nouhra E, Swenie R, Sánchez-García M, Matheny PB, Smith ME (2017) How to know the fungi: combining field inventories and DNA-barcoding to document fungal diversity. New Phytol 214(3):913–919PubMedCrossRefGoogle Scholar
  93. Truong C, Gabbarini LA, Corrales A, Mujic AB, Escobar JM, Moretto A, Smith ME (2019) Ectomycorrhizal fungi and soil enzymes exhibit contrasting patterns along elevation gradients in southern Patagonia. New Phytol. In press. https://doi.org/10.1111/nph.15714 PubMedCrossRefGoogle Scholar
  94. Valenzuela E, Leiva S, Godoy R (2001) Variación estacional y potencial enzimático de microhongos asociados con la descomposición de hojarasca de Nothofagus pumilio. Rev Chil Hist Nat 74(4):737–749Google Scholar
  95. Valenzuela E, Moreno G, Garnica S, Godoy R, Ramírez C (1999) Mycosociology in native forests of Nothofagus of the X Region of Chile, diversity and ecological role. Mycotaxon 72:217–226Google Scholar
  96. Van der Heijden MG, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310CrossRefGoogle Scholar
  97. van der Wal A, Geydan TD, Kuyper TW, de Boer W (2013) A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiol Rev 37(4):477–494PubMedCrossRefGoogle Scholar
  98. Van Schöll L, Kuyper TW, Smits MM, Landeweert R, Hoffland E, van Breemen N (2008) Rock-eating mycorrhizas: their role in plant nutrition and biogeochemical cycles. Plant Soil 303(1–2):35–47Google Scholar
  99. Weathers KC, Lovett GM, Likens GE, Caraco NF (2000) Cloudwater inputs of nitrogen to forest ecosystems in southern Chile: forms, fluxes, and sources. Ecosystems 3(6):590–595CrossRefGoogle Scholar
  100. Zúñiga-Feest A, Delgado M, Alberdi M (2010) The effect of phosphorus on growth and cluster-root formation in the Chilean Proteaceae: Embothrium coccineum (R. et J. Forst.). Plant Soil 334(1–2):113–121CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Universidad Austral de ChileValdiviaChile
  2. 2.Universidad de O’HigginsRancaguaChile

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