Structure and Diversity of Arbuscular Mycorrhizal Fungal Communities Across Spatial and Environmental Gradients in the Chaco Forest of South America

  • Gabriel GrilliEmail author
  • Nicolás Marro
  • Lucía Risio Allione
Part of the Fungal Biology book series (FUNGBIO)


The Chaco forest is one of the most diverse ecosystems in South America (SA) and harbors different vegetation units with high levels of biodiversity. However, the information about how belowground communities are spatially structured across vegetation units in the Chaco forest is scarce. We aimed to analyze the variation of taxonomic and phylogenetic diversity and the structure of the arbuscular mycorrhizal fungal communities across different vegetation units of the Chaco forest. Arbuscular mycorrhizal fungi (AMF) richness showed significant differences between vegetation units. The AMF community composition was being significantly structured by geographic variables (i.e. wider scale), environmental variables (i.e. altitude, temperature and precipitation) and edaphic (i.e. pH and Nitrogen). In addition, the AMF communities in the Chaco forest might be phylogenetically clustered compared to local (Córdoba Province), regional (SA) and global species pool. In general, a variation of AMF communities in the Chaco forest might be determined by the spatial configuration and environmental conditions.


Arbuscular mycorrhiza Chaco forest Mycorrhizal symbiosis 



This work was supported by the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), FONCYT, Universidad Nacional de Córdoba and Universidad Nacional de San Luis. We are grateful to María del Rosario Iglesias for helping with the map edition.


  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26(1):32–46Google Scholar
  2. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48CrossRefGoogle Scholar
  3. Becerra A, Bartoloni N, Cofré N, Soteras F, Cabello M (2014) Arbuscular mycorrhizal fungi in saline soils: Vertical distribution at different soil depth. Braz J Microbiol 45(2):585–594CrossRefGoogle Scholar
  4. Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632CrossRefGoogle Scholar
  5. Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153(1–2):51–68CrossRefGoogle Scholar
  6. Bucher E, Huszar P (1999) Sustainable management of the Gran Chaco of South America: ecological promise and economic constraints. J Environ Manage 57:99–108CrossRefGoogle Scholar
  7. Cabido M, Zeballos SR, Zak M, Carranza ML, Giorgis M A, Cantero JJ, Acosta AT (2018) Native woody vegetation in central Argentina: Classification of Chaco and Espinal forests. Appl Veg Sci 21(2):298–311CrossRefGoogle Scholar
  8. Caldas M, Goodin D, Sherwood S, Campos Krauer J, Wisely S (2015) Landcover change in the paraguayan chaco: 2000–2011. J Land Use Sci 10:1–18CrossRefGoogle Scholar
  9. Cagnolo L, Cabido M, Valladares G (2006) Plant species richness in the Chaco Serrano Woodland from central Argentina: ecological traits and habitat fragmentation effects. Biol Conserv 132(4):510–519CrossRefGoogle Scholar
  10. Chave J (2004) Neutral theory and community ecology. Ecol Lett 7(3):241–253CrossRefGoogle Scholar
  11. Cofré N, Becerra A, Nohura E, Soteras F (2012). Arbuscular mycorrhizae and dark-septate endophytes on Atriplex cordobensis in saline sites from Argentina. J Agric Technol 8:2201–2214Google Scholar
  12. Davison J, Öpik M, Zobel M, Vasar M, Metsis M, Moora M (2012) Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS One 7(8): e41938CrossRefGoogle Scholar
  13. 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 127(6251):970–973CrossRefGoogle Scholar
  14. Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4(3):337–345CrossRefGoogle Scholar
  15. Egan CP, Callaway RM, Hart MM, Pither J, Klironomos J (2017) Phylogenetic structure of arbuscular mycorrhizal fungal communities along an elevation gradient. Mycorrhiza 27(3):273–282CrossRefGoogle Scholar
  16. Fick SE, Hijmans RJ (2017) WorldClim 2: new 1 km spatial resolution climate surfaces for global land areas. Int J Climatol 37(12):4302–4315CrossRefGoogle Scholar
  17. Gause GF (1934) Experimental analysis of Vito Volterra’s mathematical theory of the struggle for existence. Science 79(2036):16–17CrossRefGoogle Scholar
  18. Götzenberger L, de Bello F, Bråthen KA, Davison J, Dubuis A, Guisan A, Lepš J, Lindborg R, Moora M, Pärtel M, Pellissier L, Pottier J, Vittoz P, Zobel K, Zobel M (2012) Ecological assembly rules in plant communities approaches, patterns and prospects. Biol Rev 87(1):111–127CrossRefGoogle Scholar
  19. Grilli G, Urcelay C, Galetto L (2012) Forest fragment size and nutrient availability: complex responses of mycorrhizal fungi in native–exotic hosts. Plant Ecol 213:155–165CrossRefGoogle Scholar
  20. Grilli G, Urcelay C, Galetto L (2013) Linking mycorrhizal fungi and soil nutrients to vegetative and reproductive ruderal plant development in a fragmented forest at central Argentina. Forest Ecol Manag 310:442–449CrossRefGoogle Scholar
  21. Grilli G, Urcelay C, Galetto L, Davison J, Vasar M, Saks Ü, Jairus T, Öpik M (2015) The composition of arbuscular mycorrhizal fungal communities in the roots of a ruderal forb is not related to the forest fragmentation process. Environ Microbiol 17:2709–2720CrossRefGoogle Scholar
  22. Grilli G, Longo S, Huais PY, Pereyra M, Verga EG, Urcelay C, Galetto L (2017) Fungal diversity at fragmented landscapes: synthesis and future perspectives. Curr Opin Microbiol 37:161–165CrossRefGoogle Scholar
  23. Hijmans RJ, van Etten J, Cheng J, Mattiuzzi M, Sumner M, Greenberg JA (2017) Raster: Geographic Data Analysis and Modeling. R package version 2.3–33; 2016Google Scholar
  24. Hoyos L, Cingolani A, Zak M, Vaieretti M, Gorla D, Cabido M (2013) Deforestation and precipitation patterns in the arid Chaco forests of central Argentina. Appl Veg Sci 16:260–271CrossRefGoogle Scholar
  25. Hubbell SP (2001) The unified neutral theory of species abundance and diversity. Princeton University Press, PrincetonGoogle Scholar
  26. Kauffman J, Steele M, Cummings D, Jaramillo V (2003) Biomass dynamics associated with deforestation, fire, and conversion to cattle pasture in a Mexican tropical dry forest. Forest Ecol Manag 176:1–12CrossRefGoogle Scholar
  27. Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43(11):2294–2303CrossRefGoogle Scholar
  28. Kotilínek M, Hiiesalu I, Košnar J, Šmilauerová M, Šmilauer P, Altman J, Dvorský M, Kopecký M, Doleža J (2017) Fungal root symbionts of high altitude vascular plants in the Himalayas. Scientific REPortS 7:6562. DOI: CrossRefPubMedPubMedCentralGoogle Scholar
  29. Legendre P, Anderson MJ (1999) Distance based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monograph 69 (1):1–24CrossRefGoogle Scholar
  30. Lekberg YLVA, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95(1):95–105CrossRefGoogle Scholar
  31. Longo S, Nouhra E, Goto B, Berbara R, Urcelay C (2014) Effects of fire on arbuscular mycorrhizal fungi in the Mountain Chaco Forest. Forest Ecol Manag 315:86–94CrossRefGoogle Scholar
  32. Lugo MA, Gonzalez Maza E, Cabello MN (2003) Arbuscular mycorrhizal fungi in a mountain grassland II: Seasonal variation of colonization studied, along with its relation to grazing and metabolic host type. Mycologia 95 (3):407–415CrossRefGoogle Scholar
  33. Lugo MA, Anton AM, Cabello MN (2005) Arbuscular mycorrhizas in the Larrea divaricata scrubland of the arid ‘Chaco’, Central Argentina. J Agric Technol 1(1):163–178Google Scholar
  34. McGill BJ, Maurer BA, Weiser, MD (2006) Empirical evaluation of neutral theory. Ecology 87(6):1411–1423CrossRefGoogle Scholar
  35. Menoyo E, Renison D, Becerra A (2009) Arbuscular mycorrhizas and performance of Polylepis australis trees in relation to livestock density. Forest Ecol Manag 258:2676–2682CrossRefGoogle Scholar
  36. Nori J, Torres R, Lescano J, Cordier J, Periago M, Baldo D (2016) Protected areas and spatial conservationpriorities for endemic vertebrates of the Gran Chaco, one of the most threatened ecoregions of the world. Divers Distrib 22:1212–1219CrossRefGoogle Scholar
  37. Oksanen J, Blanchet F, Kindt R, Legendre P, Minchin P, O’Hara R (2018) Vegan: Community Ecology Package. R package vegan, vers. 2.2–1; 2015Google Scholar
  38. Öpik M, Metsis M, Daniell TJ, Zobel M, Moora M (2009) Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol 184(2):424–437CrossRefGoogle Scholar
  39. Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier U, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188(1) 223–241CrossRefGoogle Scholar
  40. Öpik M, Zobel M, Cantero JJ, Davison J, Facelli JM, Hiiesalu I, Jairus T, Kalwij JM, Koorem K, Leal ME, Liira J, Metsis M, Neshataeva V, Paal J, Phosri C, Põlme S, Reier Ü, Saks Ü, Schimann H, Thiéry O, Vasar M, Moora M (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430CrossRefGoogle Scholar
  41. Oyarzabal M, Clavijo J, Oakley L, Biganzoli F, Tognetti P, Barberis I, Maturo H, Aragón R, Campanello P, Prado D, Oesterheld M, León R (2018) Unidades de vegetación de la Argentina. Ecol Austral 28:040–063CrossRefGoogle Scholar
  42. Pielou EC (1975) Ecology diversity. John Wiley and Sons.New York, p 165Google Scholar
  43. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc R Soc Lond B Biol Sci 276(1676):4237–4245CrossRefGoogle Scholar
  44. Powell JR, Rillig MC (2018) Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytol 220 (4):1059–1075CrossRefGoogle Scholar
  45. Preston FW (1948) The commonness, and rarity, of species. Ecology 29(3):254–283CrossRefGoogle Scholar
  46. Silvertown J (2004) Plant coexistence and the niche. Trends Ecol Evol 19(11):605–611CrossRefGoogle Scholar
  47. Smith S, Read D (2008) Mycorrhizal Symbiosis, third ed. Academic, LondonGoogle Scholar
  48. Soteras F, Renison D, Becerra A (2014) Restoration of high altitude forests in an area affected by a wildfire: Polylepis australis Bitt. seedlings performance after soil inoculation. Trees-Struct Funct 28:173–182CrossRefGoogle Scholar
  49. Soteras F, Grilli G, Cofré MN, Marro N, Becerra A (2015) Arbuscular mycorrhizal fungal composition in high montane forests with different disturbance histories in central Argentina. Appl Soil Ecol 85:30–37CrossRefGoogle Scholar
  50. Soteras F, Coutinho Moreira B, Grilli G, Pastor N, Carneiro Mendes F, Ruela Mendes D, Renison D, Megumi Kasuya MC, de Souza FA, Becerra A (2016) Arbuscular mycorrhizal fungal diversity in rhizosphere spores versus roots of an endangered endemic tree from Argentina: is fungal diversity similar among forest disturbance types?. Appl Soil Ecol 98:272–277CrossRefGoogle Scholar
  51. Tokeshi M (1990). Niche apportionment or random assortment: species abundance patterns revisited. J Anim Ecol 59(3):1129–1146CrossRefGoogle Scholar
  52. Urcelay C, Díaz S, Gurvich D, Chapin F, Cuevas E, Domínguez LS (2009) Mycorrhizal community resilience in response to experimental plant functional type removals in a woody ecosystem. J Ecol 97:1291–1301CrossRefGoogle Scholar
  53. van der Gast CJ, Gosling P, Tiwari B, Bending GD (2011) Spatial scaling of arbuscular mycorrhizal fungal diversity is affected by farming practice. Environ Microbiol 3(1):241–249CrossRefGoogle Scholar
  54. Verbruggen E, van Der Heijden MG, Weedon JT, Kowalchuk GA, Röling WF (2012) Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol Ecol 21(10):2341–2353CrossRefGoogle Scholar
  55. Verga EG, Sánchez Hümöller HL, Peluc SI, Galetto L (2017) Forest fragmentation negatively affects common bird species in subtropical fragmented forests. Emu-Austral Ornithol 117(4):359–369CrossRefGoogle Scholar
  56. Zak MR, Cabido M, Hodgson JG (2004) Do subtropical seasonal forests in the Gran Chaco, Argentina, have a future?. Biol Cons 120(4):589–598CrossRefGoogle Scholar
  57. Zak MR, Cabido M, Cáceres D, Díaz S (2008) What drives accelerated land cover change in central Argentina? Synergistic consequences of climatic, socioeconomic, and technological factors. J Environ Manage 42(2):181–189CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Gabriel Grilli
    • 1
    Email author
  • Nicolás Marro
    • 1
  • Lucía Risio Allione
    • 2
    • 3
  1. 1.Laboratorio de Micología. Instituto Multidisciplinario de Biología VegetalFCEFyN (CONICET-Universidad Nacional de Córdoba)CórdobaArgentina
  2. 2.Laboratorio de Micología, Diversidad e Interacciones Fúngicas (MICODIF), Área de Ecología, Facultad de Química, Bioquímica y FarmaciaUniversidad Nacional de San LuisSan LuisArgentina
  3. 3.IMIBIO-CONICET, Universidad Nacional de San LuisSan LuisArgentina

Personalised recommendations