Southern Highlands: Fungal Endosymbiotic Associations

  • Mónica A. Lugo
  • Eugenia Menoyo
Part of the Fungal Biology book series (FUNGBIO)


In South America (SA), Highlands above-treeline stretch along 7000 km in a North-South direction, occupying almost 694,000 km2, most of it is located in the Andean region except for 34,500 km2 in the Chaco region. In these Highlands are represented very particular ecoregions and phytogeographic areas in desertic, arid and semiarid biomes with characteristic vegetations composed by endemic plants. These Highlands are completely different from the ones found in Europe and Asia due to their proper biodiversity, climate, geographic position, geologic origin, and biogeography. Highlands in SA are suffering soil erosion, a retraction of their areas due to the advance of the agricultural-livestock frontiers and overgrazing, environmental deterioration by firewood extraction and the accumulation of mining toxic waste. Mountain ecosystems are huge-natural-environmental laboratories where it is possible to study important ecological unresolved hypothesis. The study of fungal-root-endophytes (mycorrhizal and dark-septate fungi), their colonization to native plants and how to enhance the resilience of soil ecosystems deserves special attention. Studies on fungal-root-endophytes have been carried out extensively worldwide; however, the research in Highlands are still scant around the world, especially in SA. This Chapter reviews and discusses fungal-root-endophytes colonization in Highlands of SA, and compared them to the worldwide knowledge.


Desertic grasslands High steppes Mountain Mycorrhizal type Root colonization 



The authors are especially grateful for his collaboration to the Biol. Esteban M. Crespo in the field works in the Highlands grasslands, Puna and Prepuna, and to the Microb. Hebe J. Iriarte (Research Technical Assistant of CONICET) for her assistance with the elaboration and improvement of the Figures. Likewise, we would like to express our gratitude to the researchers Drs. Marta Cabello and Laura Domínguez, who were pioneers and propellers of mycorrhizal fungi research of the native ecosystems in Argentina. In addition, ML wants to thank especially to her worthy director, Dr. Ana Anton for having trained her not only in the knowledge of the plants but also by the integral academic training received from her. This work was financially supported by PROICO 02-2718 (FQByF-UNSL), and both authors are staff researchers from CONICET.


  1. Aagesen L, Bena MJ, Nomdedeu S, Panizza A, López RP, Zuloaga FO (2012) Areas of endemism in the southern central Andes. Darwiniana 50:218–251Google Scholar
  2. Aagesen L, Szumik CA, Zuloaga FO, Morrone O (2009) Quantitative biogeography in the South America highlands – recognizing the Altoandina, Puna and Prepuna through the study of Poaceae. Cladistics 25:295–310CrossRefGoogle Scholar
  3. Allen MF (1991) The ecology of mycorrhizae. In: De Barnes RSK, Birks HJB, Connor EF, Harper JL, Paine R (eds). Cambridge University Press, Cambridge, New York, Port Chester, Melbourne, SydneyGoogle Scholar
  4. Angulo-Veizaga WV, García-Apaza E (2014) Baccharis incarum and fungus Arbuscular Mycorrhizal symbiotic relationship for land fallow in the Bolivian highland. CienciaAgro 3:51–58Google Scholar
  5. Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545CrossRefGoogle Scholar
  6. Barnola LG, Montilla MG (1997) Vertical distribution of mycorrhizal colonization, root hairs, and belowground biomass in three constrasting sites from the tropical high mountains, Mérida, Venezuela. Arct Antarct Alp Res 29:206–212CrossRefGoogle Scholar
  7. Bradford MA (2014) Good dirt with good friends. Nature 505:486–487CrossRefGoogle Scholar
  8. Brooks TM, Mittermeier RA, da Fonseca GAB, Gerlach J, Moffmann M, Lamoreux JF, Mittermeier CG, Pilgrim JD, Rodrigues RR (2006) Global biodiversity conservation priorities. Science 313:58–61PubMedPubMedCentralCrossRefGoogle Scholar
  9. 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 320:37–77CrossRefGoogle Scholar
  10. Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist 220:1108–1115PubMedPubMedCentralCrossRefGoogle Scholar
  11. Buytaert W, Cuesta-Camacho F, Tobón C (2011) Potential impacts of climate change on the environmental services of humid tropical alpine regions. Global Ecology and Biogeography 20(1):19–33CrossRefGoogle Scholar
  12. Cabido MR, Carranza ML, Acosta ATR, Paez S (1991) Contribución al conocimiento fitosociológico del Bosque Chaqueño Serrano en la provincia de Córdoba, Argentina. Phytocoenologia 19:547–566CrossRefGoogle Scholar
  13. Cabido MR (1985) Las comunidades vegetales de la Pampa de Achala, Sierras de Córdoba, Argentina. Documents phytosociologiques 9:431–443Google Scholar
  14. Cabido MR, Breimer R, Vega G (1987) Plant communities and associated soil types in a high plateau of the Córdoba mountains, Central Argentina. Mountain Res Develop 7:25–42CrossRefGoogle Scholar
  15. Cabido M, Giorgis M, Tourn. 2010. Guía para una excursión botánica en las Sierras de Córdoba. Boletín de la Sociedad Argentina de Botánica 45(1–2):209–219Google Scholar
  16. Cabrera AL (1976) Territorios fitogeográficos de la República Argentina. Enciclopedia Argentina de Agricultura y Jardinería, 2da. Edición, II (1). ACME, ArgentinaGoogle Scholar
  17. Cabrera AL, Willink A (1980) Biogeografía de América Latina. OEA, Washington, DCGoogle Scholar
  18. Cardoso da Silva JM and Bates JM (2002) Biogeographic Patterns and Conservation in the South American Cerrado: A tropical savanna hotspot. BioScience 52:225–233CrossRefGoogle Scholar
  19. Carvalho F, Souza FA, Carrenho R, Moreira FMS, Jesus EC, Fernandes GW (2012) The mosaic of habitats in the high-altitude Brazilian rupestrian fields is a hotspot for arbuscular mycorrhizal fungi. Appl Soil Ecol 52:9–19CrossRefGoogle Scholar
  20. Casanova-Katny MA, Torres-Mellado GA, Palfner G, Cavieres LA (2011) The best for the guest: high Andean nurse cushions of Azorella madreporica enhance arbuscular mycorrhizal status in associated plant species. Mycorrhiza 21:613–622PubMedPubMedCentralCrossRefGoogle Scholar
  21. Clarke JDA (2006) Antiquity of aridity in the Chilean Atacama Desert. Geomorphology 73:101–114CrossRefGoogle Scholar
  22. Costa HAO, Stürmer SL, Ragonezi C, Grazziotti PH, Fonseca Santos Grazziotti DC, de Barros Silva E (2016) Species richness and root colonization of arbuscular mycorrhizal fungi in Syngonanthus elegans, an endemic and threatened species from the Cerrado domain in Brazil. Ciência e Agrotecnologia 40:326–336CrossRefGoogle Scholar
  23. Coutinho ES, Fernandes GW, Berbara RLL, Valério HM, Goto BT (2015) Variation of arbuscular mycorrhizal fungal communities along an altitudinal gradient in rupestrian grasslands in Brazil. Mycorrhiza 25:627–638PubMedPubMedCentralCrossRefGoogle Scholar
  24. Díaz S, Acosta A, Cabido M (1994) Grazing and the phenology of flowering and fruiting in a montane grassland in Argentina: a niche approach. Oikos 70: 287–295CrossRefGoogle Scholar
  25. Diazgranados M, Barber JC (2017) Geography shapes the phylogeny of frailejones (Espeletiinae Cuatrec., Asteraceae): a remarkable example of recent rapid radiation in sky islands. PeerJ, PubMedPubMedCentralCrossRefGoogle Scholar
  26. Dinerstein ED, Olson M, Graham DJ, Webster AL, Primm SA, Bookbinder MP, Ledec YG (1995) Una evaluación del estado de conservación de las ecorregiones terrestres de América Latina y el Caribe. World Bank, Washington, DCGoogle Scholar
  27. Echternacht L, Trovóa M, Oliveira CT, Pirania JR (2011) Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil. Flora 206:782–791CrossRefGoogle Scholar
  28. Farley KA, Bremer LL, Harden CP, Hartsig J (2013) Changes in carbon storage under alternative land uses in biodiverse Andean grasslands: implications for payment for ecosystem services. Conservation Letters 6(1):21–27CrossRefGoogle Scholar
  29. Ferreyra M, Cingolani A, Ezcurra C, Bran D (1998) High-Andean vegetation and environmental gradients in northwestern Patagonia. Journal Vegetation Science 9:307–316CrossRefGoogle Scholar
  30. Ferreyra M, Grigera D (2002) Conservación de la vegetación altoandina en el Parque Nacional Nahuel Huapi. Jornadas Regionales Desarrollo y Ciencia en Áreas de Montaña, Universidad Nacional del ComahueGoogle Scholar
  31. Fiaschi P, Pirani J (2009) Review of plant biogeographic studies in Brazil. Journal of Systematics and Evolution 47(5):477–496CrossRefGoogle Scholar
  32. Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O’Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill J, Monfreda C, Polasky S, Rockström J, Sheehan J, Siebert S, Tilman D, Zaks DPM (2011) Solutions for a cultivated planet. Nature 478:337–342PubMedPubMedCentralCrossRefGoogle Scholar
  33. Fracchia S, Silvani V, Flachsland E, Terada G, Sede S (2014a) Symbiotic seed germination and protocorm development of Aa achalensis Schltr., a terrestrial orchid endemic from Argentina. Mycorrhiza 24:35–43CrossRefGoogle Scholar
  34. Fracchia S, Aranda-Rickert A, Flachsland E, Terada G, Sede S (2014b) Mycorrhizal compatibility and symbiotic reproduction of Gavilea australis, an endangered terrestrial orchid from south Patagonia. Mycorrhiza 24:627–634PubMedPubMedCentralCrossRefGoogle Scholar
  35. García I, Mendoza R, Pomar MC (2012) Arbuscular mycorrhizal symbiosis and dark septate endophytes under contrasting grazing modes in the Magellanic steppe of Tierra del Fuego. Agriculture, Ecosystems and Environment 155:194–201CrossRefGoogle Scholar
  36. García Romero JF, García Fernandéz DC, Correa de Restrepo M (2004) Incidencia de las Micorrizas Arbusculares y Vesículos Arbusculares como estrategia adaptativa de especies de páramo y selva Altoandina, Cordillera Oriental de Colombia. Colombia forestal 8:43–59CrossRefGoogle Scholar
  37. Gardes M, Dahlberg A (1996) Mycorrhizal diversity in arctic and alpine tundra: an open question. New Phytologist 133:147–157CrossRefGoogle Scholar
  38. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20(8):519–530PubMedCrossRefGoogle Scholar
  39. Giulietti AM, Pirani JR (1988) Patterns of geographic distribution of some plant species from the Espinhaço Range, Minas Gerais and Bahia, Brazil. In: Vanzolini PE, Heyer WR (eds) Proceedings of a Workshop on Neotropical Distribution Patterns. Academia Brasileira de Ciências, Rio de Janeiro, Brazil, 1987Google Scholar
  40. Hughes CE, Atchison GW (2015) The ubiquity of alpine plant radiations: from the Andes to the Hengduan Mountains. New Phytologist 207:275–282PubMedCrossRefPubMedCentralGoogle Scholar
  41. Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytologist 140:295–310CrossRefGoogle Scholar
  42. Knapp DG, Pintye A, Kovács GM (2012) The dark side is not fastidious-Dark septate endophytic fungi of native and invasive plants of semiarid sandy areas. PloS ONE 7:e32570PubMedPubMedCentralCrossRefGoogle Scholar
  43. Kohn LM, Stasovski E (1990) The mycorrhizal status of plants at Alexandra Fiord, Ellesmere Island, Canada, a High Arctic site. Mycologia 82:23–35CrossRefGoogle Scholar
  44. Körner C (1999) Alpine plant life. Springer-Verlag Heidelberg, New YorkCrossRefGoogle Scholar
  45. Körner C (2007) The use of “altitude” in ecological research.Trends Eco. Evol 22:569–574Google Scholar
  46. Kotilínek M, Hiiesalu I, Košnar J, Šmilauerová M, ŠmilauerP, Altman J, Dvorský M, Kopecký M, Doleža J (2017) Fungal root symbionts of high altitude vascular plants in the Himalayas. Scientific REPortS 7:6562. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Letelier L, Squeo FA, Arancio G, Marticorena A, Muñoz-Schick M, Arroyo MTK, León-Lobos P, Montecinos S, Gutiérrez JR (2008) Diversidad vegetal de la Región de Atacama, Chile. In: Squeo FA, Arancio G, Arancio G (eds) Libro Rojo de la Flora nativa y de los Sitios Prioritarios para su Conservación. Ediciones Universidad de La Serena, Chile, p 123–135Google Scholar
  48. López RP (2000) La prepuna boliviana. Ecología en Bolivia 34:45–70Google Scholar
  49. López RP, Beck S (2002) Phytogeographical affinities and life form composition of the Bolivian Prepuna. Candollea 57:77–96Google Scholar
  50. Lugo MA, Domínguez de Toledo L, Anton AM (1995) Sclerocystis sinuosa (Glomales, Zygomycetes) en cuatro Poaceae Argentinas. Kurtziana 24:145–152Google Scholar
  51. Lugo MA, Domínguez de Toledo L, Anton AM (1997) Seis especies de Glomales (Zygomycetes) en Poaceae Argentinas. I. Kurtziana 25:187–204Google Scholar
  52. Lugo MA, Cabello MN (2002) Native arbuscular mycorrhizal fungi (AMF) from mountain grassland (Córdoba, Argentina) I. Seasonal variation of fungal spore diversity. Mycologia 94 (4):579–586PubMedPubMedCentralGoogle Scholar
  53. Lugo MA, González Maza ME, Cabello MN (2003) Arbuscular mycorrhizal fungi (AMF) from native Argentinian -South American- mountain grassland II. Seasonal variation of colonization and its relation with grazing and metabolic host type. Mycologia 95:407–415CrossRefGoogle Scholar
  54. Lugo MA, Ferrero M, Menoyo E, Estévez MC, Siñeriz F, Anton AM (2008) Arbuscular mycorrhizal fungi and rhizospheric bacteria diversity along an altitudinal gradient in South American Puna grassland. Microb Ecol 55:705–713CrossRefGoogle Scholar
  55. Lugo MA, Menoyo E, Risio Allione L, Negritto MA, Henning JA, Anton AM (2018) Arbuscular mycorrhizas and dark septate endophytes associated with grasses from the Argentine Puna. Mycologia 110:654–665PubMedCrossRefPubMedCentralGoogle Scholar
  56. Lugo MA, Negritto MA, Jofré M, Anton A, Galetto L (2012) Colonization of native Andean grasses by arbuscular mycorrhizal fungi in Puna: a matter of altitude, host photosynthetic pathway and host life cycles. FEMS Microbiol Ecol 81:455–466PubMedCrossRefPubMedCentralGoogle Scholar
  57. Madriñán S, Cortés AJ, Richardson JE (2013) Páramo is the world’s fastest evolving and coolest biodiversity hotspot. Frontiers in Genetics 4:1–6CrossRefGoogle Scholar
  58. Martínez Carretero E (1995) La Puna Argentina: delimitación general y división en distritos florísticos. Bol Soc Argent Bot 31:27–40Google Scholar
  59. Martínez Carretero E, Faggi AM, Fontana JL, Aceñolaza P, Gandullo R, Cabido M, Iriart D, Prado D, Roig FA, Eskuche U (2016) Prodromus sinsistemático de la República Argentina y una breve introducción a los estudios fitosociológicos. Bol Soc Argent Bot 51:469–549Google Scholar
  60. Matteucci SD, Silva ME, Rodríguez AF (2016) Clasificaciones de la tierra: ¿provincias fitogeográficas, ecorregiones o paisajes?. Fronteras 14:1–16Google Scholar
  61. McKay CP, Friedmann EI, Gómez-Silva B, Cáceres-Villanueva L, Andersen DT, Landheim R (2003) Temperature and moisture conditions for life in the extreme arid region of the Atacama Desert: Four years of observations including the El Niño of 1997–1998. Astrobiology 3 (2):393–406PubMedCrossRefPubMedCentralGoogle Scholar
  62. Menoyo E, Becerra AG, Renison D (2007) Mycorrhizal associations in Polylepis woodlands of Central Argentina. Can J Bot 85:526–531CrossRefGoogle Scholar
  63. Monasterio M (1980) Las formaciones vegetales de los páramos de Venezuela. In: Monasterio M (ed) Estudios Ecológicos en los Páramos Andinos. Editorial de la Universidad de Los Andes, Mérida, p 93–158Google Scholar
  64. Montilla M, Herrera RA, Monasterio M (1992) Micorrizas vesiculo-arbusculares en parcelas que se encuentran en sucesión-regeneración en los Andes tropicales. Suelo y Planta 2:59–70Google Scholar
  65. Morello J, Matteucci SD, Rodríguez AF, Silva ME (2018) Ecorregiones y complejos Ecosistémicos argentines, 2da ed, FADU, GEPAMA, Orientación Gráfica Editora, ArgentinaGoogle Scholar
  66. Morong T (1891) The Flora of the Desert of Atacama. Bulletin of the Torrey Botanical Club 18 (2):39–48CrossRefGoogle Scholar
  67. Morrone JJ (2001a) Biogeografía de América Latina y el Caribe. M&T–Manuales & Tesis SEA, vol. 3. ZaragozaGoogle Scholar
  68. Morrone JJ (2001b) Toward a formal definition of the Paramo-Punan subregion and its provinces. Rev Mus Argent Cienc Nat 3:1–12CrossRefGoogle Scholar
  69. Morrone JJ (2004) Panbiogeografía, componentes bióticos y zonas de transición. Revista Brasileira de Entomologia 48(2):149–162CrossRefGoogle Scholar
  70. Morrone JJ (2006) Biogeographic areas and transition zones of Latin America and the Caribbean Islands based on panbiogeographic and cladistics analyses of the entomofauna. Annu Rev Entomol 51:467–494PubMedCrossRefPubMedCentralGoogle Scholar
  71. Morrone JJ (2014) Biogeographical regionalisation of the Neotropical region. Zootaxa 3782:1–110PubMedCrossRefPubMedCentralGoogle Scholar
  72. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefGoogle Scholar
  73. Manuel-Navarrete D, Gallopín GC, Blanco M, Díaz-Zorita M, Ferraro DO, Herzer H, Laterra P, Murmis MR, Podestá GP, Rabinovich J, Satorre EH, Torres F, Viglizzo EF (2007) Multi-causal and integrated assessment of sustainability: the case of agriculturization in the Argentine Pampas. Environ Dev Sustain 11:621–638CrossRefGoogle Scholar
  74. Nogueira RE, Liparini Pereira O, Megumi Kasuya MC, da Silva Lanna MC, Pimentel Mendonça M (2005) Fungos micorrízicos associados a orquídeas em campos rupestres na região do Quadrilátero Ferrífero, MG, Brasil. Acta Bot Bras 19:417–424CrossRefGoogle Scholar
  75. Navone S, Bosio MJ (2008–2009) Región PUNA. Centro de Investigación y Aplicación de la Teledetección CIATE, Facultad de Agronomía – Universidad de Buenos Aires, Reports 2008–2009,
  76. Oehl F, Körner C (2014) Multiple mycorrhization at the coldest place known for Angiosperm plant life. Alpine Botany 124:193–198CrossRefGoogle Scholar
  77. Oki Y, Goto BT, Jobim K, Rosa LH, Costa Ferreira M, Silva Coutinho E, de Azevedo Xavier JH, Fernanda Carvalho, de Souza Moreira FM, de Souza FA, Louro Berbara RL, Fernandes GW (2016) Arbuscular Mycorrhiza and Endophytic Fungi in Ruspestrian Grasslands. In: GW Fernandes (ed) Ecology and Conservation of Mountain top Grasslands in Brazil, Springer, Switzerland., p 157–179CrossRefGoogle Scholar
  78. Olson DM, Dinerstein E (2002) The global 200: priority ecoregions for global conservation. Ann Missuri Bot Garden 89:199–224CrossRefGoogle Scholar
  79. Orchard S, Hilton S, Bending GD, Dickie IA, Standish RJ, Gleeson DB, Jeffery RP, Powell JR, Walker C, Bass D, Monk J, Simonin A, Ryan MH (2017) Fine endophytes (Glomus tenue) are related to Mucoromycotina, not Glomeromycota. New Phytologist 213:481–485PubMedCrossRefPubMedCentralGoogle Scholar
  80. Overbeck GE, Vélez-Martin E, Scarano FR, Lewinsohn TM, Fonseca CR, Meyer ST, Muller SC, Ceotto P, Dadalt L, Durigan G, Gislene G, Gossner MM, Guadagnin DL, Lorenzen K, Jacobi CM, Weisser WW, Pillar VD (2015) Conservation in Brazil needs to include non-forest ecosystems. Diversity Distrib 21:1455–1460CrossRefGoogle Scholar
  81. Oyarzabal M, Clavijo J, Oakley L, Biganzoli F, Tognetti P, Barberis I, Maturo HM, Aragón R, Campanello PI, Prado D, Oesterheld M, León RJC (2018) Unidades de vegetación de la Argentina. Ecología Austral 28:40–63CrossRefGoogle Scholar
  82. Pagano MC, Scotti MR (2009) A survey of the arbuscular mycorrhiza occurrence in Paepalanthus bromelioides and Bulbostylis sp. in rupestrian fields, Brazil. Micologia Aplicada Internacional 21:1–10Google Scholar
  83. Pagano MC, Cabello MN (2012) Occurrence of mycorrhizas in Highland fields. In: Pagano MC (ed) Mycorrhiza: Occurrence in Natural and Restored Environments. NOVA Science Publishers Inc., New York, p 87–98Google Scholar
  84. Peterson RL, Massicotte HB, Melville L (2004) Mycorrhizas: anatomy and cell biology. NRC Research Press and CABI Publishing, Ottawa and WallingfordGoogle Scholar
  85. Peyre G, Balslev H, Font X (2018) Phytoregionalisation of the Andean páramo. PeerJ PeerJ 6:e4786. CrossRefPubMedPubMedCentralGoogle Scholar
  86. Pliscoff P, Zanetta N, Hepp J, Machuca J (2017) Efectos sobre la flora y vegetación (del evento de precipitación extremo de agosto 2015 en Alto Patache, Desierto de Atacama, Chile. Revista de Geografía Norte Grande 68:91–103Google Scholar
  87. Posadas PE, Estévez JM, Morrone JJ (1997) Distributional patterns and endemism areas of vascular plants in the Andean subregion. Fontqueria 48:1–10Google Scholar
  88. Prado DE (1993a) What is the Gran Chaco vegetation in South America? I. A review. Contribution to the study of flora and vegetation of the Chaco. V. Candollea 48:145–172Google Scholar
  89. Prado DE (1993b) What is the Gran Chaco vegetation in South America? II. A redefinition. Contribution to the study of flora and vegetation of the Chaco. VII. Candollea 48:615–629Google Scholar
  90. Prado DE, Gibbs PE (1993) Patterns in species distribution in the dry seasonal forest of South America. Annals Missouri Botanical Garden 80:902–927CrossRefGoogle Scholar
  91. Rapini A, Ribeiro PL, Lambert S, Pirani JR (2008) A flora dos campos rupestres da Cadeia do Espinhaço. Megadiversidade 4:15–23Google Scholar
  92. Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391CrossRefGoogle Scholar
  93. Read DJ, Haselwandter K (1981) Observations on the mycorrhizal status of some alpine plant communities. New Phytologist 88:341–352CrossRefGoogle Scholar
  94. Read DJ, Pérez Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytologist 157:475–492CrossRefGoogle Scholar
  95. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581CrossRefGoogle Scholar
  96. Renison D, Cuyckens GAE, Pacheco S, Guzmán GF, Grau HR, Marcora P, Robledo G, Cingolani AM, Dominguez J, Landi M, Bellis L, Hensen I (2013) Distribución y estado de conservación de las poblaciones de árboles y arbustos del género Polylepis (Rosaceae) en las montañas de Argentina. Ecología Austral 23:27–36Google Scholar
  97. Ruggiero RM, Ezcurra C (2003) Regiones y transiciones biogeográficas: complementaridad de los análisis en biogeografía histórica y ecológica. In: Morrone JJ, Llorente Bousquets J (eds) Una Perspectiva Latinoamericana de la Biogeografía de México. Prensas Científicas, UNAM, México DF, p 141–154Google Scholar
  98. Ruotsalainen AL, Eskelinen A (2011) Root fungal symbionts interact with mammalian herbivory, soil nutrient availability and specific habitat conditions. Oecologia 166:807–817PubMedCrossRefPubMedCentralGoogle Scholar
  99. Ruthsatz B (1977). Pflanzengesellschaften und ihre Lebensbedingungen in den Andinen Halbwüsten Nordwest-Argentiniens. J. Cramer, VaduzGoogle Scholar
  100. Ruthsatz B, Movia CP (1975) Relevamiento de las estepas andinas del noreste de la Provincia de Jujuy, Argentina. Fundación para la Educación, la Ciencia y la Cultura, Buenos AiresGoogle Scholar
  101. Salvarredi LA, Crespo EM, Menoyo E, Filippa EM, Barboza GE, Lugo MA (2010) Micorrizas arbusculares y endófitos septados oscuros en gentianaceae nativas de la Argentina. Bol Soc Argent Bot 45:223–229Google Scholar
  102. Schmidt SK, Sobieniak-Wiseman LC, Kageyama SA, Halloy SRP, Schadt CW (2008) Mycorrhizal and dark-septate fungi in plant roots above 4270 meters elevation in the Andes and Rocky Mountains. Arct Antarct Alp Res 40:576–583CrossRefGoogle Scholar
  103. Silvani V, Rothen C, Rodríguez MA, Cisneros G, Godeas A, Aranda-Rickert A, Fracchia S (2013) Fungal root colonization of Puccinellia frigida (Phil.) Johnston, a dominant grass species inhabiting the margins of high-altitude hypersaline Andean wetlands. Aquatic Botany 108:26–32CrossRefGoogle Scholar
  104. Sklenář P, Hedberg I, Cleef AM (2014) Island biogeography of tropical alpine floras. Journal of Biogeography 41(2):287–297. CrossRefGoogle Scholar
  105. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic press, Cambridge, UKGoogle Scholar
  106. Squeo FA, Arroyo MTK, Marticorena A, Arancio G, Muñoz-Schick M, Negritto M, Rojas G, Rosas M, Rodríguez R, Humaña AM, Barrera E, Marticorena C (2008) Catálogo de la Flora Vascular de la Región de Atacama. In: Squeo FA, Arancio G, Arancio G (eds) Libro Rojo de la Flora nativa y de los Sitios Prioritarios para su Conservación. Ediciones Universidad de La Serena, Chile, p 67–120Google Scholar
  107. Trappe JM (1987) Phylogenetic and ecologic aspects of mycotrophy in the Angiosperms from and Evolutionary standpoint. In: Safir GR (ed) Ecophysiology of VA Mycorrhizal Plants. CRC Press, Boca Raton, FL, p 5–25Google Scholar
  108. Urcelay C, Acho J, Joffre R (2011) Fungal root symbionts and their relationship with fine root proportion in native plants from the Bolivian Andean highlands above 3700 m elevation. Mycorrhiza 21:323–330PubMedCrossRefPubMedCentralGoogle Scholar
  109. Urcelay C (2002) Co-ocurrence of three fungal root symbionts in Gaultheria poeppiggi DC in Central Argentina. Mycorrhiza 12:89–92CrossRefGoogle Scholar
  110. Vásquez DL, Balslev H, Sklenář P (2015) Human impact on tropical-alpine plant diversity in the northern Andes. Biodiversity and Conservation 24(11):2673–2683CrossRefGoogle Scholar
  111. Velázquez MS, Stürmer SL, Bruzone C, Fontenla S, Barrera M, Cabello M (2016) Occurrence of arbuscular mycorrhizal fungi in high altitude sites of the Patagonian Altoandina region in Nahuel Huapi National Park (Argentina). Acta Botanica Brasilica 30 (4):521–531CrossRefGoogle Scholar
  112. Veldman JW, Overbeck GE, Negreiros D, Mahy G, Le Stradic S, Fernandes GW, Durigan G, Buisson E, Putz FE, Bond WJ (2015) Where tree planting and forest expansion are bad for biodiversity and ecosystem services. BioScience 347:484–485Google Scholar
  113. Viglizzo EF, Jobbágy E (eds) (2010) Expansión de la Frontera Agropecuaria en Argentina y su Impacto Ecológico-Ambiental. Ministerio de Agricultura, Ganadería y Pesca de la Nación. Ediciones INTAGoogle Scholar
  114. Wahl A-L, Spiegelberg T (2016) Arbuscular mycorrhizal fungi in changing mountain grassland ecosystems- a challenge for research. Botany 94:435–458CrossRefGoogle Scholar
  115. Walker C, Gollotte A, Redecker D (2018a) A new genus, Planticonsortium (Mucoromycotina), and new combination (P. tenue), for the fine root endophyte, Glomus tenue (basionym Rhizophagus tenuis). Mycorrhiza 28:213–219CrossRefGoogle Scholar
  116. Walker C, Harper CJ, Brundrett MC, Krings M (2018b) Looking for Arbuscular Mycorrhizal Fungi in the Fossil Record: An Illustrated Guide. In: Krings M, Cúneo NR, Harper CJ, Rothwell G (eds) Transformative Paleobotany. AP, Elsevier, p 481–517CrossRefGoogle Scholar
  117. Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363CrossRefGoogle Scholar
  118. Young BE, Josse C, Stern M, Vasconez S, Olander J, Smyth R, Zador M, Sánchez de Lozada A, Comer PJ, Moull K, Echavarría M, Hak J (2015) Hotspot de biodiversidad de los Andes tropicales. In: Resumen técnico del perfil del ecosistema. Washington, D.C.: NatureServer & EcoDecisiónGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Mónica A. Lugo
    • 1
  • Eugenia Menoyo
    • 2
  1. 1.Biological Sciences, National University of San LuisGrupo MICODIF (Micología, Diversidad e Interacciones Fúngicas)/IMIBIO (Instituto Multidisciplinario de Investigaciones Biológicas)-CONICET-CCT SLSan LuisArgentina
  2. 2.National University of San Luis, Grupo MICODIF (Micología, Diversidad e Interacciones Fúngicas)-UNSL/IMASL (Instituto de Matemática Aplicada San Luis)-CONICETSan LuisArgentina

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