Agroforestry Systems

, Volume 92, Issue 2, pp 555–574 | Cite as

Effects of soil physical and chemical parameters, and farm management practices on arbuscular mycorrhizal fungi communities and diversities in coffee plantations in Colombia and Mexico

  • Raúl Hernando Posada
  • Marina Sánchez de Prager
  • Gabriela Heredia-Abarca
  • Ewald Sieverding
Article

Abstract

Arbuscular mycorrhizal fungi (AMF) are essential for growth of coffee plants in acidic and phosphate deficient soils in Central and South America. We investigated the species richness of Glomeromycotean fungi in 9–13 years old coffee plantations in Colombia and Mexico. Fungal species richness was related to physical and chemical soil factors, soil aggregate stability, and farm management practices. Using morphological spore characteristics 85 AMF species were found. AMF species similarity within the plantations was 62–73 %, and the most regularly AMF species found in both countries were: Acaulospora mellea, Acaulospora spinosa, Ambispora fennica, Diversispora aurantia, Dominikia aurea, Glomus brohultii, Rhizoglomus clarum and Rhizoglomus intraradices. In both countries species richness was differently influenced by agronomic management intensity and soil parameter. In Colombia, where soils were more fertile with higher organic matter and soil pH than in Mexico, soil parameter explained the variations in species diversity, while in Mexico, agronomic management intensities explained the variations in species richness among sites. Soil aggregate stability slightly explains the AMF species richness in Colombia and Mexico. It can be concluded that the Glomeromycotean species richness is very high in older coffee plantations in Colombia and Mexico, and that agronomic inputs have positive effects on species richness in very acidic soils with lower organic matter contents, while in more fertile soils like in Colombia, soil parameter define more the AMF richness.

Keywords

Arbuscular mycorrhiza Farm management intensity Edaphic parameters Water stable aggregates Spore diversity Bait cultures 

Notes

Acknowledgments

The authors express their thanks to Nubia Rodriguez, Fernando Ramos and Felipe Vergara in Colombia; and to Rosa Arias and Alvaro Ihuicamina in Mexico for their collaboration in laboratory activities. Thanks to Anita Antoninka who gave advice on the statistical models. Thanks also to the CONACyT [Grant NO.14646 Reg 213551] (México) and OAS for the scholarship grant support for the principle author and to the Institute of Ecology A.C. for the logistical support.

References

  1. Allen MF, Swenson W, Querejeta JI, Egerton-Warburton LM, Treseder KK (2003) Ecology of mycorrhizae: a conceptual framework for complex interactions among plants and fungi. Ann Rev Phytopathol 41:271–303. doi: 10.1146/annurev.phyto.41.052002.095518 CrossRefGoogle Scholar
  2. Álvarez-Sánchez J, Johnson NC, Antoninka A, Chaudhary VB, Lau MK, Owen SM, Sánchez-Gallen I, Guadarrama P, Castillo S (2011) Large-scale diversity patterns in spore communities of arbuscular mycorrhizal fungi. In: Pagano MC (ed) Mycorrhiza: occurrence and role in natural and restored environments. Nova Science Publishers, Hauppauge, pp 33–50Google Scholar
  3. Al-Yahyaʼei MN, Oehl F, Vallino M, Lumini E, Redecker D, Wiemken A, Bonfante P (2011) Unique arbuscular mycorrhizal fungal communities uncovered in date palm plantations and surrounding desert habitats of Southern Arabia. Mycorrhiza 21:195–209. doi: 10.1007/s00572-010-0323 CrossRefPubMedGoogle Scholar
  4. Andrade SAL, Mazzafera P, Schiavinato MA, Silveira APD (2009) Arbuscular mycorrhizal association in coffee. J Agric Sci 147:105–115. doi: 10.1017/S0021859608008344 CrossRefGoogle Scholar
  5. Arbuckle JL (2010) Amos 18 User’s Guide, 1st edn. SPSS Inc, CrawfordvilleGoogle Scholar
  6. Arias RM, Heredia-Abarca G, Sosa VJ, Fuentes-Ramírez LE (2012) Diversity and abundance of arbuscular mycorrhizal fungi spores under different coffee production systems and in a tropical montane cloud forest patch in Veracruz, Mexico. Agrofor Syst 85:179–193. doi: 10.1007/s10457-011-9414-3 CrossRefGoogle Scholar
  7. Augé R (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  8. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. doi: 10.1016/j.tplants.2012.04.001 CrossRefPubMedGoogle Scholar
  9. Blaszkowski J (2012) Glomeromycota. Polish Academy of Science, KrakowGoogle Scholar
  10. Bolaños BMM, Rivillas-Osorio CA, Suárez-Vásquez S (2000) Identificación de micorrizas arbusculares en suelos de la zona cafetera Colombiana. Rev Cenicafé 51:245–262Google Scholar
  11. Bollen KA (1989) Structural equations with latent variables. Wiley, New YorkCrossRefGoogle Scholar
  12. Bouyoucos GJ (1962) Hydrometer method Improved for making particle size analyses of soils. Agron J 54:464–465CrossRefGoogle Scholar
  13. Brundrett M, Peterson L, Melville L, Addy H, McGonigle T, Schaffer G, Bougher N, Massicotte H (1994) Practical methods in mycorrhiza research. Mycologue Publications, WaterlooGoogle Scholar
  14. Camargo JC, Feijoo A, Zúñiga MC, Cardona H, Gaviria J (2005) Silvopastoral systems with isolated timber trees within pastures in the Coffee region of Colombia. Livest Res Rural Dev 17:1–13Google Scholar
  15. 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 CrossRefPubMedGoogle Scholar
  16. Cardoso IM, Boddington C, Janssen BH et al (2003) Distribution of mycorrhizal fungal spores in soils under agroforestry and monocultural coffee systems in Brazil. Agrofor Syst 58:33–43. doi: 10.1023/A:1025479017393 CrossRefGoogle Scholar
  17. Castillo CG, Borie FR, Godoy R, Rubio R, Sieverding E (2006) Diversity of arbuscular mycorrhizal plant species and fungal species in evergreen forest, deciduous forest and grassland ecosystems of Southern Chile. J Appl Bot Food Qual 80:40–47Google Scholar
  18. Codazzi A (1998) Consideraciones generales para interpretar análisis de suelos. IGAC, BogotáGoogle Scholar
  19. Codazzi A (2009) Estudio general de suelos y zonificación de tierras, Departamento de Risaralda. Instituto Geográfico Agustín Codazzi, BogotaGoogle Scholar
  20. Da Silva IR, de Mello CMA, Ferreira Neto RA, da Silva DKA, de Melo AL, Oehl F, Maia LC (2014) Diversity of arbuscular mycorrhizal fungi along an environmental gradient in the Brazilian semiarid. Appl Soil Ecol 84:166–175. doi: 10.1016/j.apsoil.2014.07.008 CrossRefGoogle Scholar
  21. de Almeida VC, Nogueira MI, Guimarães RJ, Mourão Júnior M (2003) Carbono da biomassa microbiana e micorriza en solo sub mata nativa e agroecossistemas cafeeiros. Acta Sci Agron 25:147–153. doi: 10.4025/actasciagron.v28i1.1289 Google Scholar
  22. de Beenhouwer M, Van Geel M, Ceulemans T et al (2015) Changing soil characteristics alter the arbuscular mycorrhizal fungi communities of Arabica coffee (Coffea arabica) in Ethiopia across a management intensity gradient. Soil Biol Biochem 91:133–139. doi: 10.1016/j.soilbio.2015.08.037 CrossRefGoogle Scholar
  23. de Carvalho AMX, de Castro Tavares R, Cardoso IM, Kuyper TW (2010) Mycorrhizal associations in agroforestry systems. In: Patrice D (ed) Soil bioloy and agriculture in the tropics, 1st edn. Springer, Heidelberg, pp 185–208CrossRefGoogle Scholar
  24. de Souza RG, da Silva DKA, de Mello CMA, Goto BT, da Silva FSB, Sampaio EVSB, Maia LC (2013) Arbuscular mycorrhizal fungi in revegetated mined dunes. Land Deg Env 24:147–155. doi: 10.1002/ldr.1113 CrossRefGoogle Scholar
  25. del Mar Alguacil M, Díaz-Pereira E, Caravaca F, Fernández DA, Roldán A (2009) Increased diversity of arbuscular mycorrhizal fungi in a long-term field experiment via application of organic amendments to a semiarid degraded soil. App Env Microbiol 75:4254–4263. doi: 10.1128/AEM.00316-09 CrossRefGoogle Scholar
  26. Duponnois R, Plenchette C, Thioulouse J, Cadet P (2001) The mycorrhizal soil infectivity and arbuscular mycorrhizal fungal spore communities in soils of different aged fallows in Senegal. Appl Soil Ecol 17:239–251. doi: 10.1007/s00572-010-0357-8 CrossRefGoogle Scholar
  27. Fixen PE, Grove JH (1990) Soil testing and plant analysis. In: Westerman RL (ed) Testing soils for phosphorus. Soil Science Society America, Madison, pp 141–180Google Scholar
  28. Furrazola E, Herrera-Peraza R, Kaonongbua W, Bever JD (2010) Glomus candidum, a new species of arbuscular mycorrhizal fungi from North American grassland. Mycotaxon 113:101–109CrossRefGoogle Scholar
  29. Geissert D, Ibáñez A (2008) Calidad y ambiente físico–químico de los suelos. In: Manson R, Hernández-Ortiz V, Gallina S, Mehltreter K (eds) Agroecosistemas Cafetaleros de Veracruz: biodiversidad, manejo y conservación. Instituto de Ecología A.C, Xalapa, pp 213–222Google Scholar
  30. Gómez-Ramírez M, Resendiz-Espinosa IN (2002) Seguimiento de nortes en el litoral del Golfo de México en la temporada 1999–2000. Revista Geográfica 131:5–19Google Scholar
  31. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, New YorkCrossRefGoogle Scholar
  32. Grace JB, Keeley JE (2006) A structural equation model analysis of postfire plant diversity in California Shrublands. Ecol Appl 16:503–514CrossRefPubMedGoogle Scholar
  33. Grace JB, Pugesek BH (1998) On the use of path analysis and related procedures for the investigation of ecological problem. Am Nat 152:151–159CrossRefPubMedGoogle Scholar
  34. Guzmán O, Jaramillo A (1989) Estudio climático de Risaralda y Quindío. Bol Tec Cenicafé 15:1–64Google Scholar
  35. Hazard C, Gosling P, van der Gast CJ, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of Arbuscular mycorrhizal fungi at the landscape scale. ISME J 7:498–508. doi: 10.1038/ismej.2012.127 CrossRefPubMedGoogle Scholar
  36. Hempel S, Renker C, Buscot F (2007) Differences in the species composition of Arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9:1930–1938CrossRefPubMedGoogle Scholar
  37. Hernández-Martínez G, Manson RH, Contreras A (2009) Quantitative classification of coffee agroecosystems spanning a range of production intensities in Central Veracruz, México. Agric Ecosyst Environ 134:89–98CrossRefGoogle Scholar
  38. Hodge A (2014) Interactions between arbuscular mycorrhizal fungi and organic material substrates. In: Hodge A (ed) Advances in applied microbiology, vol 89. Elsevier Inc, London, pp 47–100Google Scholar
  39. Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nat 413:297–299. doi: 10.1038/35095041 CrossRefGoogle Scholar
  40. Hua J, Jiang Q, Bai J, Ding F, Lin X, Yin Y (2014) Interactions between arbuscular mycorrhizal fungi and fungivorous nematodes on the growth and arsenic uptake of tobacco in arsenic-contaminated soils. Appl Soil Ecol 84:176–184. doi: 10.1016/j.apsoil.2014.07.004 CrossRefGoogle Scholar
  41. Johnson NC, Pfleger FL (1992) Vesicular-arbuscular mycorrhizae and cultural stresses. In: Bethlenfalvay GJ, Linderman RG (eds) Mycorrhizae in sustainable agriculture. American Society of Agronomy, Madison, pp 71–99Google Scholar
  42. Koide RT (1991) Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol 117:365–386CrossRefGoogle Scholar
  43. Lagos JA (2004) Guías de laboratorio, Asignatura: suelos. Programa Ingeniería Ambiental. Universidad Libre, BogotáGoogle Scholar
  44. Landis FC, Gargas A, Givnish TJ (2004) Relationships among arbuscular mycorrhizal fungi, vascular plants and environmental conditions in oak savannas. New Phytol 164:493–504. doi: 10.1111/j.1469-8137.2004.01202.x CrossRefGoogle Scholar
  45. Lara L (2003) Diversidad y actividad de hongos micorrizicos-arbusculares, en agroecosistemas cafetaleros perturbados por la erosión. MSc. Dissertation, Universidad de ColimaGoogle Scholar
  46. Lewis P, Malcolm B, Steed G (2006) Conservation crop farming: farm management perspective. University of Melbourne, MelbourneGoogle Scholar
  47. Liu Z, Fu B, Zheng X, Liu G (2010) Plant biomass, soil water content and soil N:P ratio regulating soil microbial functional diversity in a temperate steppe: a regional scale study. Soil Biol Biochem 42:445–450. doi: 10.1016/j.soilbio.2009.11.027 CrossRefGoogle Scholar
  48. Mäder P, Fließbach A, Dubois D, Gunst L, Fried P (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697CrossRefPubMedGoogle Scholar
  49. Manns HR, Maxwell CD, Emery RJN (2007) The effect of ground cover or initial organic carbon on soil fungi, aggregation, moisture and organic carbon in one season with oat (Avena sativa) plots. Soil Till Res 96:83–94. doi: 10.1016/j.still.2007.03.001 CrossRefGoogle Scholar
  50. Martínez-García LB, Armas C, Miranda JDD, Padilla FM, Pugnaire FI (2010) 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 CrossRefGoogle Scholar
  51. McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software Design, Gleneden BeachGoogle Scholar
  52. Miller SP (2000) Arbuscular mycorrhizal colonization of semi-aquatic grasses along a wide hydrologic gradient. New Phytol 145:145–155. doi: 10.1046/j.1469-8137.2000.00566.x CrossRefGoogle Scholar
  53. Miller SP, Bever JD (1999) Distribution of Arbuscular mycorrhizal fungi in stands of the wetland grass Panicum hemitomon along a wide hydrologic gradient. Oecologia 119:586–592CrossRefPubMedGoogle Scholar
  54. Mirás-Avalos JM, Antunes PM, Koch A, Khosla K, Klironomos JN, Dunfield KE (2011) The influence of tillage on the structure of rhizosphere and root-associated Arbuscular mycorrhizal fungal communities. Pedobiol 54:235–241. doi: 10.1016/j.pedobi.2011.03.005 CrossRefGoogle Scholar
  55. Montiel RB, Robledo MJD (1998) Caracterización, descripción y evaluación de especies frutales en el banco genético del CRUO. MSc. Dissertation, Universidad VeracruzanaGoogle Scholar
  56. Moreno CE (2001) Métodos para medir la biodiversidad. Gorfi S.A, ZaragosaGoogle Scholar
  57. Muleta D, Assefa F, Nemomissa S, Granhall U (2007) Composition of coffee shade tree species and density of indigenous Arbuscular mycorrhizal fungi (AMF) spores in Bonga natural coffee forest, southwestern Ethiopia. For Ecol Manage 241:145–154. doi: 10.1016/j.foreco.2007.01.021 CrossRefGoogle Scholar
  58. Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Env Microbiol 69:2816–2824CrossRefGoogle Scholar
  59. Oehl F, Sieverding E, Mäder P, Dubois D, Ineichen K, Boller T, Wiemken A (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583CrossRefPubMedGoogle Scholar
  60. Oehl F, Sieverding E, Ineichen K, Mäder P, Wiemken A, Boller T (2009) Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agric Ecosyst Environ 134:257–268. doi: 10.1016/j.agee.2009.07.008 CrossRefGoogle Scholar
  61. Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, van der Heijden M, Sieverding E (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 CrossRefGoogle Scholar
  62. Oehl F, da Silva GA, Goto BT, Sieverding E (2011a) Glomeromycota: three new genera and glomoid species reorganized. Mycotaxon 116:75–120. doi: 10.5248/116.75 CrossRefGoogle Scholar
  63. Oehl F, Sieverding E, Palenzuela J, Ineichen K, Alves da Silva G (2011b) Advances in Glomeromycota taxonomy and classification. IMA Fungus 2:191–199. doi: 10.5598/imafungus.2011.02.02.10 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Peña-Vanegas CP, Cardona GI, Mazorra A, Arguellez JH, Arcos AL (2006) Micorrizas arbusculares de la Amazonia colombiana, catálogo ilustrado. Instituto Amazonico de Investigaciones Científicas—SINCHI, Bogotá Google Scholar
  65. Porcel R, Gómez M, Kaldenhoff R, Ruiz-Lozano J (2005) Impairment of NtAQP1 gene expression in tobacco plants does not affect root colonization pattern by arbuscular mycorrhizal fungi but decreases their symbiotic efficiency under drought. Mycorrhiza 15:417–423CrossRefPubMedGoogle Scholar
  66. Posada R, Sieverding E (2014) Arbuscular mycorrhiza in Colombian coffee plantations fertilized with coffee pulps as organic manure. J Appl Bot Food Qual 87:243–248. doi: 10.5073/JABFQ.2014.087.034 Google Scholar
  67. Posada RH, Prager MS, Sieverding E, Dorantes KA (2012) Relaciones entre los hongos filamentosos y solubilizadores de fosfatos con algunas variables edáficas y el manejo de cafetales. Rev Biol Trop 60:1075–1096PubMedGoogle Scholar
  68. Ramírez MM (2014) Evaluación de la diversidad de Hongos Formadores de Micorrizas Arbusculares (HFMA) y su relación con el establecimiento de simbiosis con Physalis peruviana L. PhD. Dissertation, Universidad Nacional de ColombiaGoogle Scholar
  69. Rilling MC, Wright SF, Eviner VT (2002) The role of Arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species. Plant Soil 238:325–333CrossRefGoogle Scholar
  70. Saif SR (1983) The influence of soil aeration on the efficiency of vesicular-arbuscular mycorrhizae. II. Effect of soil oxygen on the growth and mineral uptake in Eupatorium odoratum L., Sorghum bicolor (L.) Moench and Guizotia abyssinica (L.f.) Cass. inoculated with vesicular-arbuscular mycorrhizal fungi. New Phytol 95:405–417CrossRefGoogle Scholar
  71. Sánchez de Prager M (1999) Endomicorrizas en agroecosistemas colombianos. Universidad Nacional de Colombia—Sede Palmira, Cali-ColombiaGoogle Scholar
  72. Sánchez de Prager M, Posada RH, Velásquez D, Narvaez M (2010) Metodologías básicas para el trabajo con micorriza arbuscular y hongos formadores de micorriza arbuscular. Universidad Nacional de Colombia, PalmiraGoogle Scholar
  73. Sánchez C, Montilla E, Rivera R, Cupull R (2005) Comportamiento de 15 cepas de hongos micorrizogenos (HMA) sobre el desarrollo de posturas de cafeto en un suelo pardo gleyzoso. Rev For Latinoam 38:83–95Google Scholar
  74. Sanders IR (2004) Plant and arbuscular fungal diversity—are we looking at the relevant levels of diversity and are we using the right techniques? New Phytol 164:415–418CrossRefGoogle Scholar
  75. Schenck NC, Pérez I (1990) Manual for the identification of VA mycorrhizal fungi. Synergistic Publications, GainesvilleGoogle Scholar
  76. Shipley B (2000) Cause and correlation in biology: a user’s guide to path analysis, structural equations and causal Inference. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  77. Sieverding E (1991) Vesicular-arbuscular mycorrhiza management in tropical agrosystems. Deutsche Gesellschaft fur Technische Zusammenarbeit, EschbornGoogle Scholar
  78. Sieverding E, Oehl F (2005) Are arbuscular mycorrhizal fungal species invasive—derived from our knowledge about their distribution in different ecosystems?. In: BCPC Symposium Proceedings No. 81: Plant protection and plant health in Europe: introduction and spread of invasive species. Monograph series, The British Crop Protection Council, Alton, pp 197–202Google Scholar
  79. Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro) aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31CrossRefGoogle Scholar
  80. Stötefeld L, Scheu S, Rohlfs M (2012) Fungal chemical defence alters density-dependent foraging behaviour and success in a fungivorous soil arthropod. Ecol Entomol 37:323–329. doi: 10.1111/j.1365-2311.2012.01373.x CrossRefGoogle Scholar
  81. Stürmer SL, Siqueira JO (2011) Species richness and spore abundance of arbuscular mycorrhizal fungi across distinct land uses in Western Brazilian Amazon. Mycorrhiza 21:255–267CrossRefPubMedGoogle Scholar
  82. Stutz JC, Morton JB (1996) Successive pot cultures reveal high species richness of arbuscular endomycorrhizal fungi in arid ecosystems. Can J Bot 74:1883–1889CrossRefGoogle Scholar
  83. Tisdall JM (1991) Fungal hyphae and structural stability of soil. Aust J Soil Res 29:729–743CrossRefGoogle Scholar
  84. Vaast P, Zasoski RJ, Bledsoe CS (1996) Effects of vesicular-Arbuscular mycorrhizal inoculation at different soil P availabilities on growth and nutrient uptake of in vitro propagated coffee (Coffea arabica L.) plants. Mycorrhiza 6:493–497. doi: 10.1007/s005720050153 CrossRefGoogle Scholar
  85. van der Heijden MG, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nat 396:69–72CrossRefGoogle Scholar
  86. Violi H, Barrientos-Priego A, Wright S, Escamilla-Prado E, Morton J, Menge J, Lovatt C (2008) Disturbance changes arbuscular mycorrhizal fungal phenology and soil glomalin concentrations but not fungal spore composition in montane rainforests in Veracruz and Chiapas, Mexico. For Ecol Manag 254:276–290. doi: 10.1016/j.foreco.2007.08.016 CrossRefGoogle Scholar
  87. Wang MY, Hu LB, Wang WH, Liu ST, Li M, Liu RJ (2009) Influence of long-term fixed fertilization on diversity of arbuscular mycorrhizal fungi. Pedosphere 19:663–672. doi: 10.1016/S1002-0160(09)60161-2 CrossRefGoogle Scholar
  88. Wetzel K, Da Silva G, Matczinski U, Oehl F, Fester T (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 72:88–96CrossRefGoogle Scholar
  89. Whitcomb S, Stutz JC (2007) Assessing diversity of arbuscular mycorrhizal fungi in a local community: role of sampling effort and spatial heterogeneity. Mycorrhiza 17:429–437CrossRefPubMedGoogle Scholar
  90. Wu F, Dong M, Liu Y, Ma X, An L, Young JPW, Feng H (2011) Effects of long-term fertilization on AM fungal community structure and Glomalin-related soil protein in the Loess Plateau of China. Plant Soil 342:233–247. doi: 10.1007/s11104-010-0688-4 CrossRefGoogle Scholar
  91. Yoder RE (1936) A direct method of aggregate analysis and study of physical nature of erosion losses. J Am Soc Agron 28:337–351CrossRefGoogle Scholar
  92. Zar JH (1999) Biostatistical analysis. Prentice Hall, New JerseyGoogle Scholar
  93. Zhao ZW, Xia YM, Qin XZ, Li XW, Cheng LZ, Sha T, Wang GH (2001) Arbuscular mycorrhizal status of plants and the spore density of arbuscular mycorrhizal fungi in the tropical rain forest of Xishuangbanna, Southwest China. Mycorrhiza 11:159–162. doi: 10.1007/s005720100117 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Raúl Hernando Posada
    • 1
    • 4
  • Marina Sánchez de Prager
    • 2
  • Gabriela Heredia-Abarca
    • 1
  • Ewald Sieverding
    • 3
  1. 1.Instituto de Ecología A.C. Carretera antigua a CoatepecXalapaMexico
  2. 2.Universidad Nacional de ColombiaPalmira, Valle del CaucaColombia
  3. 3.Institute of Plant Production and Agroecology in the Tropics and SubtropicsUniversity of HohenheimStuttgart HohenheimGermany
  4. 4.ZenKinoko SAS.BogotáColombia

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