Skip to main content

Advertisement

SpringerLink
Log in

Predictors of Arbuscular Mycorrhizal Fungal Communities in the Brazilian Tropical Dry Forest

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Arbuscular mycorrhizal fungi (AMF) are symbiotic fungi with a broad distribution, and many taxa have physiological and ecological adaptations to specific environments, including semiarid ecosystems. Our aim was to address regional distribution patterns of AMF communities in such semiarid environments based on spore morphological techniques. We assessed AMF spores at the bottom and top of inselbergs distributed throughout the tropical dry forest in the Northeast region of Brazil. Across 10 replicate inselbergs and the surrounding area, spanning a range of altitude between 140 and 2000 m, we scored the AMF soil diversity and properties in 52 plots. We fitted parsimonious ordination analyses and variance partitioning models to determine the environmental factors which explained the variation in AMF community, based on morphological spore analysis. The diversity of AMF was similar at the bottom and top of inselbergs; however, we detected high variation in abundance and richness across sites. We formulated a parsimonious richness model that used physical soil factors as predictors. The AMF community structure could be best explained through the variables coarse and total sand, iron, organic matter, potassium, silt, and sodium which together accounted for 17.8% of total variance. Several AMF species were indicators of either deficiency or high values of specific soil properties. We demonstrated that habitat isolation of the inselbergs compared with surrounding areas did not trigger differences in AMF communities in semiarid regions of Brazil. At the regional scale, soil predictors across sites drove the distribution of symbiotic mycorrhizal fungi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Santos R, Barbosa A, Almeida H, et al. (2011) Structure and floristics of a remnant of arboreous caatinga in Juvenília, northern Minas Gerais, Brazil. Cerne 17:247–258

    Article  Google Scholar 

  2. Prado D (2003) As Caatingas da América do Sul. In: Lea I, Tabarelli M, Silva J (eds) Ecol. e Conserv. da Caatingas, 1st ed. Editora Universitária da UFPE, Recife, pp 3–74

  3. Porembski S, Martinelli G, Ohlemuller R, Barthlott W (1998) Diversity and ecology of saxicolous vegetation mats on inselbergs in the Brazilian Atlantic rainforest. Divers Distrib 4:107–119. doi:10.1046/j.1365-2699.1998.00013.x

    Article  Google Scholar 

  4. Pires GG, dos Santos RM, Tristão RA, et al. (2014) Influência de variáveis ambientais na comunidade arbórea de inselbergs. Cerne 20:97–104. doi:10.1590/S0104-77602014000100013

    Article  Google Scholar 

  5. Camargo-Ricalde SL, Esperón-Rodríguez M (2005) Efecto de la heterogeneidad espacial y estacional del suelo sobre la abundancia de esporas de hongos micorrizógenos arbusculares en el valle semiárido de Tehuacán-Cuicatlán, México. Rev Biol Trop 53:339–352. doi:10.4067/S0718-16202007000300006

    Article  PubMed  Google Scholar 

  6. Klironomos J, Zobel M, Tibbett M, et al. (2011) Forces that structure plant communities: quantifying the importance of the mycorrhizal symbiosis. New Phytol 189:366–370. doi:10.1111/j.1469-8137.2010.03550.x

    Article  PubMed  Google Scholar 

  7. Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754. doi:10.1111/j.1461-0248.2004.00620.x

    Article  Google Scholar 

  8. Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411. doi:10.1016/S0169-5347(00)89157-0

    Article  CAS  PubMed  Google Scholar 

  9. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42. doi:10.1007/s005720100097

    Article  Google Scholar 

  10. Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Lett 8:214–217. doi:10.1098/rsbl.2011.0874

    Article  PubMed  Google Scholar 

  11. Veresoglou SD, Halley JM, Rillig MC (2015) Extinction risk of soil biota. Nat Commun 6:1–10. doi:10.1038/ncomms9862

    Article  Google Scholar 

  12. Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545. doi:10.1038/nature12901

    Article  CAS  PubMed  Google Scholar 

  13. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53. doi:10.1111/j.1469-8137.2006.01750.x

    Article  CAS  PubMed  Google Scholar 

  14. Klironomos JN, McCune J, Hart M, Neville J (2000) The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecol Lett 3:137–141. doi:10.1046/j.1461-0248.2000.00131.x

    Article  Google Scholar 

  15. Rosendahl S (2008) Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytol 178:253–266. doi:10.1111/j.1469-8137.2008.02378.x

    Article  PubMed  Google Scholar 

  16. Wubet T, Weiß M, Kottke I, et al. (2004) Molecular diversity of arbuscular mycorrhizal fungi in Prunus africana, an endangered medicinal tree species in dry Afromontane forests of Ethiopia. New Phytol 161:517–528. doi:10.1046/j.1469-8137.2003.00924.x

    Article  CAS  Google Scholar 

  17. Martínez-García LB, Richardson SJ, Tylianakis JM, et al. (2015) Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development. New Phytol 205:1565–1576. doi:10.1111/nph.13226

    Article  PubMed  Google Scholar 

  18. Xu T, Veresoglou SD, Chen Y, et al. (2016) Plant community, geographic distance and abiotic factors play different roles in predicting AMF biogeography at the regional scale in northern China. Environ Microbiol Rep 8:1048–1057. doi:10.1111/1758-2229.12485

    Article  CAS  PubMed  Google Scholar 

  19. Overby ST, Owen SM, Hart SC, et al. (2015) Soil microbial community resilience with tree thinning in a 40-year-old experimental ponderosa pine forest. Appl Soil Ecol 93:1–10. doi:10.1016/j.apsoil.2015.03.012

    Article  Google Scholar 

  20. Säle V, Aguilera P, Laczko E, et al. (2015) Impact of conservation tillage and organic farming on the diversity of arbuscular mycorrhizal fungi. Soil Biol Biochem 84:38–52. doi:10.1016/j.soilbio.2015.02.005

    Article  Google Scholar 

  21. Wetzel K, Silva G, Matczinski U, et al. (2014) Superior differentiation of arbuscular mycorrhizal fungal communities from till and no-till plots by morphological spore identification when compared to T-RFLP. Soil Biol Biochem 72:88–96. doi:10.1016/j.soilbio.2014.01.033

    Article  CAS  Google Scholar 

  22. Vályi K, Mardhiah U, Rillig MC, Hempel S (2016) Community assembly and coexistence in communities of arbuscular mycorrhizal fungi. ISME J 10:2341–2351. doi:10.1038/ismej.2016.46

    Article  PubMed  PubMed Central  Google Scholar 

  23. 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 Soil 368:507–518. doi:10.1007/s11104-012-1531-x

    Article  CAS  Google Scholar 

  24. Lekberg Y, Koide RT, Rohr JR, et al. (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105. doi:10.1111/j.1365-2745.2006.01193.x

    Article  Google Scholar 

  25. Sikes BA, Powell JR, Rillig MC (2010) Deciphering the relative contributions of multiple functions within plant–microbe symbioses. Ecol Model 91:1591–1597

    Article  Google Scholar 

  26. Jansa J, Erb A, Oberholzer HR, et al. (2014) Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Mol Ecol 23:2118–2135. doi:10.1111/mec.12706

    Article  CAS  PubMed  Google Scholar 

  27. Pasternak Z, Al-Ashhab A, Gatica J, et al. (2013) Spatial and temporal biogeography of soil microbial communities in arid and semiarid regions. PLoS One 8:e69705. doi:10.1371/journal.pone.0069705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Dumbrell AJ, Nelson M, Helgason T, et al. (2010) Idiosyncrasy and overdominance in the structure of natural communities of arbuscular mycorrhizal fungi: is there a role for stochastic processes? J Ecol 98:419–428. doi:10.1111/j.1365-2745.2009.01622.x

    Article  Google Scholar 

  29. Ab’Sáber AN (1999) Dossiê Nordeste seco. Estud Avançados 13:5–59

    Google Scholar 

  30. Velloso AL, Giulietti AM, Oren DC, et al (2002) Ecorregiões—Propostas para o Bioma Caatinga. In: Recife APNE, Nat. Conserv. do Bras. p 80

  31. Gomes P, Alves M (2009) Floristic and vegetational aspects of an inselberg in the semi-arid region of Northeast Brazil Edinburgh. J Bot 66:329. doi:10.1017/S0960428609005241

    Google Scholar 

  32. Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244. doi:10.1016/S0007-1536(63)80079-0

    Article  Google Scholar 

  33. Jenkins W (1964) A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Dis Rep 48:692

    Google Scholar 

  34. Hijmans RJ, Cameron SE, Parra JL, et al. (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. doi:10.1002/joc.1276

    Article  Google Scholar 

  35. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280. doi:10.1007/s004420100716

    Article  PubMed  Google Scholar 

  36. Oksanen AJ, Blanchet FG, Friendly M, et al (2016) The Vegan Package. Community Ecol. Packag

  37. Legendre P (2008) Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. J Plant Ecol 1:3–8. doi:10.1093/jpe/rtm001

    Article  Google Scholar 

  38. Cáceres M, Jansen F (2015) Package “ indicspecies ”—relationship between species and groups of sites

  39. Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna,

    Google Scholar 

  40. Öpik M, Vanatoa A, Vanatoa E, et al. (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241. doi:10.1111/j.1469-8137.2010.03334.x

    Article  PubMed  Google Scholar 

  41. Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303. doi:10.1016/j.soilbio.2011.07.012

    Article  CAS  Google Scholar 

  42. Martínez-García LB, Armas C, Miranda J de D, et al. (2011) Shrubs influence arbuscular mycorrhizal fungi communities in a semi-arid environment. Soil Biol Biochem 43:682–689. doi:10.1016/j.soilbio.2010.12.006

    Article  Google Scholar 

  43. Davison J, Moora M, Opik M, et al. (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973. doi:10.1126/science.aab1161

    Article  CAS  PubMed  Google Scholar 

  44. Pontes J, Oehl F, Marinho F, et al. (2017) Diversity of arbuscular mycorrhizal fungi in Brazil’s Caatinga and experimental agroecosystems. Biotropica, In Press

  45. Chaudhary VB, O’Dell TE, Rillig MC, Johnson NC (2014) Multiscale patterns of arbuscular mycorrhizal fungal abundance and diversity in semiarid shrublands. Fungal Ecol 12:32–43. doi:10.1016/j.funeco.2014.06.003

    Article  Google Scholar 

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

    Article  Google Scholar 

  47. Taylor A, Walker C, Bending GD (2013) Dimorphic spore production in the genus Acaulospora. Mycoscience 55:1–4. doi:10.1016/j.myc.2013.03.001

    Article  Google Scholar 

  48. Antoninka AJ, Ritchie ME, Johnson NC (2015) The hidden Serengeti—mycorrhizal fungi respond to environmental gradients. Pedobiologia (Jena) 58:165–176. doi:10.1016/j.pedobi.2015.08.001

    Article  Google Scholar 

  49. Porembski S (2007) Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Rev Bras Bot 30:579–586. doi:10.1590/S0100-84042007000400004

    Article  Google Scholar 

  50. Diaz HF, Grosjean M, Graumlich L (2003) Climate variability and change in high elevation regions: past, present and future. Clim Chang 59:1–4. doi:10.1023/A:1024416227887

    Article  Google Scholar 

  51. Soethe N, Lehmann J, Engels C (2008) Nutrient availability at different altitudes in a tropical montane forest in Ecuador. J Trop Ecol 24:397–406. doi:10.1017/S026646740800504X

    Article  Google Scholar 

  52. Koske RE, Tews LL (1987) Vesicular-arbuscular mycorrhizal fungi of Wisconsin sandy soils. Mycologia 79:901. doi:10.2307/3807694

    Article  Google Scholar 

  53. Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecology and species richness. Trends Ecol Evol 19:639–644. doi:10.1016/j.tree.2004.09.011

    Article  PubMed  Google Scholar 

  54. Treseder KK, Maltz MR, Hawkins BA, et al. (2014) Evolutionary histories of soil fungi are reflected in their large-scale biogeography. Ecol Lett 17:1086–1093. doi:10.1111/ele.12311

    Article  PubMed  Google Scholar 

  55. Brown J (1995) Macroecology. The University of Chicago Press, Chicago,

    Google Scholar 

  56. Svenning J-C, Skov F (2005) The relative roles of environment and history as controls of tree species composition and richness in Europe. J Biogeogr 32:1019–1033. doi:10.1111/j.1365-2699.2005.01219.x

    Article  Google Scholar 

  57. Duivenvoorden JF (2002) ECOLOGY: beta diversity in tropical forests. Science 295(80):636–637. doi:10.1126/science.295.5555.636

    Article  CAS  PubMed  Google Scholar 

  58. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415. doi:10.1016/j.soilbio.2008.05.021

    Article  CAS  Google Scholar 

  59. de Gannes V, Eudoxie G, Bekele I, Hickey WJ (2015) Relations of microbiome characteristics to edaphic properties of tropical soils from Trinidad. Front Microbiol 6:1–13. doi:10.3389/fmicb.2015.01045

    Article  Google Scholar 

  60. Thougnon Islas AJ, Hernandez Guijarro K, Eyherabide M, et al. (2016) Can soil properties and agricultural land use affect arbuscular mycorrhizal fungal communities indigenous from the Argentinean Pampas soils? Appl Soil Ecol 101:47–56. doi:10.1016/j.apsoil.2016.01.005

    Article  Google Scholar 

  61. Oehl F, Laczko E, Bogenrieder A, et al. (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42:724–738. doi:10.1016/j.soilbio.2010.01.006

    Article  CAS  Google Scholar 

  62. Pumpanen J, Ilvesniemi H, Hari P (2003) A process-based model for predicting soil carbon dioxide efflux and concentration. Soil Sci Soc Am J 67:402. doi:10.2136/sssaj2003.4020

    Article  CAS  Google Scholar 

  63. Chaudhary VB, Lau MK, Johnson NC (2008) Macroecology of microbes—biogeography of the Glomeromycota. Mycorrhiza. Springer, Berlin, pp. 529–563

    Chapter  Google Scholar 

  64. Hu Y, Rillig MC, Xiang D, et al. (2013) Changes of AM fungal abundance along environmental gradients in the arid and semi-arid grasslands of northern China. PLoS One 8:e57593. doi:10.1371/journal.pone.0057593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Marschner H (2011) Mineral nutrition of higher plants, third. Academic Press, London,

    Google Scholar 

  66. Subbarao GV, Ito O, Berry WL, Wheeler RM (2003) Sodium—a functional plant nutrient. CRC Crit Rev Plant Sci 22:391–416. doi:10.1080/748638747

    Google Scholar 

  67. Gattward JN, Almeida AAF, Souza JO, et al. (2012) Sodium-potassium synergism in Theobroma cacao: stimulation of photosynthesis, water-use efficiency and mineral nutrition. Physiol Plant 146:350–362. doi:10.1111/j.1399-3054.2012.01621.x

    Article  CAS  PubMed  Google Scholar 

  68. Campanelli A, Ruta C, De MG, Morone-Fortunato I (2013) The role of arbuscular mycorrhizal fungi in alleviating salt stress in Medicago sativa L. var icon. Symbiosis 59:65–76. doi:10.1007/s13199-012-0191-1

    Article  Google Scholar 

  69. Krishnasamy K, Bell R, Ma Q (2014) Wheat responses to sodium vary with potassium use efficiency of cultivars. Front Plant Sci 5:631. doi:10.3389/fpls.2014.00631

    Article  PubMed  PubMed Central  Google Scholar 

  70. Castelletti C, Santos A, Tabarelli M, Silva J (2003) Quanto ainda resta da Caatinga? Uma estimativa preliminar. In: Leal I, Tabarelli M, Silva J (eds) Ecol. e Conserv. da Caatinga, First. Recife, pp 719–734

  71. Caravaca F, Alguacil MM, Vassileva M, et al. (2004) AM fungi inoculation and addition of microbially-treated dry olive cake-enhanced afforestation of a desertified Mediterranean site. Land Degrad Dev 15:153–161. doi:10.1002/ldr.600

    Article  Google Scholar 

  72. Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 2:563–569. doi:10.1111/j.1438-8677.2009.00308.x

    Google Scholar 

  73. Mardukhi B, Rejali F, Daei G, et al. (2015) Mineral uptake of mycorrhizal wheat ( Triticum aestivum L.) under salinity stress. Commun Soil Sci Plant Anal 46:343–357. doi:10.1080/00103624.2014.981271

    Article  CAS  Google Scholar 

  74. Johnson NC, Tilman D, Wedin D (1992) Plant and soil controls on mycorrhizal fungal communities. Ecology 73:2034–2042. doi:10.2307/1941453

    Article  Google Scholar 

  75. de Assis DMA, Oehl F, Gonçalves CM, et al. (2016) Community structure of arbuscular mycorrhizal fungi in fluvial and maritime dunes of Brazilian Northeast. Appl Soil Ecol 108:136–146. doi:10.1016/j.apsoil.2016.07.018

    Article  Google Scholar 

  76. Hart MM, Reader RJ (2002) Does percent root length colonization and soil hyphal length reflect the extent of colonization for all AMF? Mycorrhiza 12:297–301. doi:10.1007/s00572-002-0186-5

    Article  PubMed  Google Scholar 

  77. Varela-Cervero S, López-García Á, 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. doi:10.1007/s00572-016-0687-2

    Article  PubMed  Google Scholar 

  78. Klironomos JN, Hart MM (2002) Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum. Mycorrhiza 12:181–184. doi:10.1007/s00572-002-0169-6

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Coordenação de aperfeiçoamento de pessoal de nível superior (CAPES), proc.: 1374510, and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), proc.: 206415/2014-1 for financial support of the research and authors’ collaboration.

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Ciências Biológicas, Departamento de Micologia, Universidade Federal de Pernambuco, Av. da Engenharia s/n, Cidade Universitária, Recife, Pernambuco, Brazil

    Natália M. F. Sousa & Leonor C. Maia

  2. Institut für Biologie, Freie Universität Berlin, Altensteinstr 6, 14195, Berlin, Germany

    Stavros D. Veresoglou

  3. Ecotoxicology, Agroscope Reckenholz—Agroscope, Wädenswil, CH-8820, Zürich, Switzerland

    Fritz Oehl & Matthias C. Rillig

  4. Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Altensteinstr. 34, 14196, Berlin, Germany

    Matthias C. Rillig

Authors
  1. Natália M. F. Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stavros D. Veresoglou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fritz Oehl
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matthias C. Rillig
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Leonor C. Maia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natália M. F. Sousa.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(DOCX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sousa, N.M.F., Veresoglou, S.D., Oehl, F. et al. Predictors of Arbuscular Mycorrhizal Fungal Communities in the Brazilian Tropical Dry Forest. Microb Ecol 75, 447–458 (2018). https://doi.org/10.1007/s00248-017-1042-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-1042-7

Keywords

Search

Navigation