Ecology and Biogeography of Arbuscular Mycorrhizal Fungi Belonging to the Family Gigasporaceae in La Gran Sabana Region (Guayana Shield), Venezuela

  • Milagros Lovera
  • Gisela Cuenca
  • Pablo Lau
  • Jesús Mavárez
Part of the Fungal Biology book series (FUNGBIO)


Arbuscular mycorrhizal fungi (AMF) play a crucial role in ecosystem functioning by improving plant nutrition and resistance to environmental stress. In La Gran Sabana (LGS), a high plateau belonging to the Venezuelan Guayana Shield, with vegetation mainly composed by savannas intermixed with forests, shrublands, meadows and palm swamps, the AMF are determinant for plant survival due to the acidic, sandy and oligotrophic nature of its soils. In this region a high diversity of species of Gigasporaceae has been found and four species discovered there (Scutellospora spinosissima, S. crenulata, S. striata, S. tepuiensis), and some undescribed morphotypes, are considered endemic. In this work, some ecological and historical factors possibly involved with the restricted distribution of these species are evaluated. The elevated plant endemism and the particular edaphic conditions present in shrublands appear like the main drivers of the important diversification processes within Gigasporaceae detected in LGS. The monophyletic origin of some of these endemic Gigasporaceae suggests that their endemism could be the result of a process of in situ diversification combined with limitations for dispersal and/or establishment in other regions. These findings and the presence of a basal lineage for the family allows proposing LGS as an evolutionary hotspot for Gigasporaceae.


AMF Dispersion Endemic species Glomeromycota Scutellospora Diversification 



We are grateful to Grisel Velázquez, who prepared the map with the sampling locations and Pedro Borges, who kindly read the manuscript and offered helpful comments and English reviews. We also thank Parupa Scientific Station (PSS) for their logistic support in La Gran Sabana during the previous field work in which the information analyzed in this study was collected.


  1. Berry PE, Huber O, Holst BK (1995) Floristic analysis and phytogeography. In: Steyermark JA, Berry PE, Holst BK (eds) Flora of the Venezuelan Guayana, Vol 1: Introduction. Missouri Botanical Garden, St Louis & Timber Press, Portland, ORGoogle Scholar
  2. Blaszkowski J (2012) Glomeromycota. W. Szafer Institute of Botany Polish Academy of Sciences, Kraków, p 304Google Scholar
  3. Briceño HO, Schubert C (1990) Geomorphology of the Gran Sabana, Guayana Shield, southeastern Venezuela. Geomorphology 3:125–141CrossRefGoogle Scholar
  4. Brown JH, Lomolino MV (1998) Biogeography. 2nd ed. Sinauer Associates, Inc., Sunderland, Massachusetts, xii + 691 pGoogle Scholar
  5. Chagnon P, Bradlley RL, Klironomos JN (2015) Trait-based partner selection drives mycorrhizal network assembly. Oikos 124:1609–1616CrossRefGoogle Scholar
  6. Chagnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Science 18:484–491CrossRefGoogle Scholar
  7. Chaudhary VB, Cuenca G, Johnson NC (2017) Tropical-temperate comparison of landscape-scale arbuscular fungal species distributions. Diversity and Distributions 2017:1–13Google Scholar
  8. Chaudhary VB, Lau MK, Johnson NC (2008) Macroecology of microbes. Biogeography of the Glomeromycota. In: Varma A (ed) Mycorrhiza. Springer-Verlag, Berlin HeidelbergGoogle Scholar
  9. Cuenca G, De Andrade Z, Escalante G (1998) Diversity of Glomalean spores from natural disturbed and revegetated communities growing on nutrient-poor tropical soils. Soil Biology and Biochemistry 30:711–719CrossRefGoogle Scholar
  10. Cuenca G, Herrera-Peraza RA (2008) Scutellospora striata sp nov, a newly described glomeromycotan fungus from La Gran Sabana, Venezuela. Mycotaxon 105:79–87Google Scholar
  11. Cuenca G, Lovera M (1992) Vesicular-arbuscular mycorrhizae in disturbed and revegetated sites from La Gran Sabana, Venezuela. Canadian Journal of Botany 70:73–79CrossRefGoogle Scholar
  12. Cuenca G, Lovera M (2010) Seasonal variation and distribution at different soil depths of arbuscular mycorrhizal fungi spores in a tropical sclerophyllous shrubland. Botany 88:54–64CrossRefGoogle Scholar
  13. Cuenca G, Lovera M, De Andrade Z, Meneses E (2003) Why are so diverse the Scutellospora at La Gran Sabana Venezuela? Proceedings of the 4th International Conference on Mycorrhizae ICOM 4 Montreal, Quebec, Canada p 593Google Scholar
  14. 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 349:970–973CrossRefGoogle Scholar
  15. De Andrade Z, Furrazola E, Cuenca G (2017) Scutellospora tepuiensis sp. nov. from the highland tepuis of Venezuela. Mycotaxon 132:9–18CrossRefGoogle Scholar
  16. de Souza TAF, Rodriguez-Echeverría S, de Andrade LA, Freitas H (2016) Arbuscular mycorrhizal fungi in Mimosa tenuiflora (Willd.) Poir from Brazilian semi-arid. Brazilian J Microbiol 47 (2):359–366CrossRefGoogle Scholar
  17. Drumbell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2009) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME Journal 1–9Google Scholar
  18. Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063CrossRefGoogle Scholar
  19. Fölster H, Dezzeo N (1994) La degradación de la vegetación. In: Ecología de la altiplanicie de la Gran Sabana (Guayana Venezolana) I. Investigaciones sobre la dinámica bosque-sabana en el sector S-E: Subcuencas de los ríos Yuruaní, Arabapó y Alto Kukenán. Dezzeo N (ed) Scientia Guaianae N°4. Caracas, VenezuelaGoogle Scholar
  20. Hart M, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytologist 153:335–344CrossRefGoogle Scholar
  21. Herrera-Peraza RA, Cuenca G, Walker C (2001) Scutellospora crenulata a new species of Glomales from La Gran Sabana Venezuela. Canadian Journal of Botany 79: 674–678CrossRefGoogle Scholar
  22. Huber O (1994) Arbustales. In: Ecología de la altiplanicie de la Gran Sabana (Guayana Venezolana) I. Investigaciones sobre la dinámica bosque-sabana en el sector S-E: Subcuencas de los ríos Yuruaní, Arabapó y Alto Kukenán. Dezzeo N (ed) Scientia Guaianae N°4. Caracas, VenezuelaGoogle Scholar
  23. Huber O (1995) Vegetation. In: Steyermark JA, Berry PE, Holst BK (eds) Flora of the Venezuelan Guayana, Vol 1: Introduction. Missouri Botanical Garden, St Louis & Timber Press, Portland, ORGoogle Scholar
  24. Huber O (2006) Herbaceous ecosystems on the Guayana Shield, a regional overview. Journal of Biogeography 33:464–475CrossRefGoogle Scholar
  25. Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 185(3):631–647CrossRefGoogle Scholar
  26. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart M, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882CrossRefGoogle Scholar
  27. Kivlin SN, Hawkes CV, Treseder K (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biology & Biochemistry 43:2294–2303CrossRefGoogle Scholar
  28. Kivlin SN, Winston GC, Goulden ML, Treseder KK (2014) Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecology 12:14–25CrossRefGoogle Scholar
  29. Landis FC, Gargas A, Givnish TJ (2004) Relationships among arbuscular mycorrhizal fungi vascular plants and environmental conditions in oak savannas. New Phytologist 164 (3):493–504CrossRefGoogle Scholar
  30. Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. Journal of Ecology 95:95–105CrossRefGoogle Scholar
  31. Lovera M (2012) Filogenia molecular de especies de hongos micorrízicos arbusculares del género Scutellospora presentes en La Gran Sabana (Edo. Bolívar, Venezuela). MSc Thesis, Center for Advanced Studies, IVIC, Caracas, 91 pGoogle Scholar
  32. Lovera M, Cuenca G (1996) Arbuscular mycorrhizal infection in Cyperaceae and Gramineae from natural, disturbed and restored savannas in La Gran Sabana, Venezuela. Mycorrhiza 6:111–118CrossRefGoogle Scholar
  33. Lovera M, Cuenca G (2007) Diversidad de hongos micorrrízicos arbusculares (HMA) y potencial micorrízico del suelo de una sabana natural y una sabana perturbada de La Gran Sabana, Venezuela. Interciencia 32:108–114Google Scholar
  34. Maherali H, Klironomos JN (2012) Phylogenetic and Trait-Based Assembly of Arbuscular Mycorrhizal Fungal Communities. PLoS ONE 7 (5):e36695CrossRefGoogle Scholar
  35. Marinho F, Silva GA, Ferreira ACA, Veras JSN, Sousa NMF, Goto BT, Maia L, Oehl F (2014) Bulbospora minima, a new genus and a new species in the Glomeromycetes from semi-arid Northeast Brazil. Sydowia 66:313–323Google Scholar
  36. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) vegan: Community Ecology Package version 2.5–2Google Scholar
  37. 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 Phytologist 184:424–437CrossRefGoogle Scholar
  38. Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist 188:223–241CrossRefGoogle Scholar
  39. Pärtel M, Öpik M, Moora M, Tedersoo L, Szava-Kovats R, Rosendahl S, Rillig MC, Lekberg Y, Kreft H, Helgason T, Eriksson O, Davison J, de Bello F, Caruso T, Zobel M (2017) Historical biome distribution and recent human disturbance shape the diversity of arbuscular mycorrhizal fungi. New Phytologist 216 (1):227–238CrossRefGoogle Scholar
  40. Peña-Venegas CP, Cardona Vanegas GI, Mazorra Valderrama A (2006) Micorrizas arbusculares de la Amazonia colombiana. Catálogo ilustrado. Publicación del Instituto Amazónico de Investigaciones Científicas, SINCHI., Editorial Scripto Ltda., Colombia, 90 pGoogle Scholar
  41. Pereira CMR, Silva DKA, Goto BT, Rosendahl S, Maia L (2018) Management practices may led to loss of arbuscular mycorrhizal fungal diversity in protected areas of the Brazilian Atlantic Forest. Fungal Ecology 34:50–58CrossRefGoogle Scholar
  42. Redecker D, Schüssler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23 (7):515–31CrossRefGoogle Scholar
  43. Rosales J, Cuenca G, Ramírez N, De Andrade Z (1997) Native colonizing species and degraded land restoration in La Gran Sabana, Venezuela. Restoration Ecology 3:147–155CrossRefGoogle Scholar
  44. Rull V, Vegas-Villarrubia T, Montoya E (2016) The neotropical Gran Sabana region: palaeoecology and conservation. The Holocene 26 (7):1162–1167CrossRefGoogle Scholar
  45. Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum the Glomeromycota: phylogeny and evolution. Mycological Research 105:1413–1421CrossRefGoogle Scholar
  46. Silva DKA, Freitas NO, Cuenca G, Maia LC, Oehl F (2008) Scutellospora pernambucana, a new fungal species in the Glomeromycetes with a characteristic germination orb. Mycotaxon 106:361–370Google Scholar
  47. Stürmer SL, Bever JD, Morton JB (2018a) Biogeography of arbuscular mycorrhizal fungi (Glomeromycota): a phylogenetic perspective on species distribution patterns. Mycorrhiza 28 (7):587–603CrossRefGoogle Scholar
  48. Stürmer SL, Kemmelmeier K, Moreira BC, Kasuya MCM, Pereira GMD, Silva K. (2018b) Arbuscular mycorrhizal fungi (Glomeromycota) communities in tropical savannas of Roraima, Brazil. Mycological Progress 17 (10):1149–1159CrossRefGoogle Scholar
  49. Veresoglou SD, Caruso T, Rillig MC (2013) Modelling the environmental and soil factors that shape the niches of two common arbuscular mycorrhizal fungal families. Plant and Soil 368:507–518CrossRefGoogle Scholar
  50. Walker C, Cuenca G, Sánchez F (1998) Scutellospora spinosissima sp. nov. a newly described Glomalean fungus from low nutrient communities in Venezuela. Annals Botany 82:721–725CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Milagros Lovera
    • 1
  • Gisela Cuenca
    • 1
  • Pablo Lau
    • 2
  • Jesús Mavárez
    • 3
    • 4
  1. 1.Centro de Ecología, Instituto Venezolano de Investigaciones Científicas (IVIC)CaracasVenezuela
  2. 2.Centro de Agroecología Tropical, Universidad Nacional Experimental Simón Rodríguez (UNESR)CaracasVenezuela
  3. 3.Laboratoire d’Ecologie AlpineUMR 5553 CNRS-Université Grenoble AlpesGrenobleFrance
  4. 4.Departamento de Ciencias Biológicas y AmbientalesUniversidad Jorge Tadeo LozanoBogotáColombia

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