Agricultural practices indirectly influence plant productivity and ecosystem services through effects on soil biota

Ecological Applications

Volumn 24, Issue 7, 2014, Pages 1842-1853

  Köhl, Luise ^a,b   Oehl, Fritz ^a   Van Der Heijden, Marcel G A ^a,b,c  

^a AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Agricultural practice; AMF; Arbuscular mycorrhiza; Conservation tillage; Ecosystem services; Extraradical hyphae; Glomeromycota; Grassland; Soil management; Soil microbial communities; Tillage

Indexed keywords

AGRICULTURAL PRACTICE; COMMUNITY STRUCTURE; ECOSYSTEM SERVICE; FUNGUS; PLANT COMMUNITY; SOIL BIOTA; TILLAGE;

GLOMEROMYCOTA;

AGRICULTURE; ANIMAL; ASTERACEAE; BIOMASS; CLOVER; ECOSYSTEM; GROWTH, DEVELOPMENT AND AGING; LOLIUM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT ROOT; PLANTAGO;

AGRICULTURE; ANIMALS; ASTERACEAE; BIOMASS; ECOSYSTEM; LOLIUM; MYCORRHIZAE; PLANT ROOTS; PLANTAGO; SOIL MICROBIOLOGY; TRIFOLIUM;

EID: 84901343225     PISSN: None     EISSN: 19395582     Source Type: Journal    
DOI: 10.1890/13-1821.1     Document Type: Article

References (85)

1. Alguacil, M. M., E. Lumini, A. Roldan, J. R. Salinas-Garcia, P. Bonfante, and V. Bianciotto. 2008. The impact of tillage practices on arbuscular mycorrhizal fungal diversity in subtropical crops. Ecological Applications 18:527-536.
2. Altieri, M. A. 1999. The ecological role of biodiversity in agroecosystems. Agriculture, Ecosystems and Environment 74:19-31.
3. Andrade, D. S., A. Colozzi-Filho, and K. E. Giller. 2003. The soil microbial community and soil tillage. Pages 51-81 in A. El Titi, editor. Soil tillage in agroecosystems. CRC Press, Boca Raton, Florida, USA.
4. Avio, L., E. Pellegrino, E. Bonari, and M. Giovannetti. 2006. Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytologist 172:347-357.
5. Barber, N. A., E. T. Kiers, N. A. Theis, R. V. Hazzard, and L. S. Adler. 2013. Linking agricultural practices, mycorrhizal fungi, and traits mediating plant-insect interactions. Ecological Applications 23:1519-1530.
6. Boddington, C. L., and J. C. Dodd. 2000. The effect of agricultural practices on the development of indigenous arbuscular mycorrhizal fungi. I. Field studies in an Indonesian ultisol. Plant and Soil 218:137-144.
7. Borie, F., R. Rubio, J. L. Rouanet, A. Morales, G. Borie, and C. Rojas. 2006. Effects of tillage systems on soil characteristics, glomalin and mycorrhizal propagules in a Chilean Ultisol. Soil and Tillage Research 88:253-261.
8. Borriello, R., E. Lumini, M. Girlanda, P. Bonfante, and V. Bianciotto. 2012. Effects of different management practices on arbuscular mycorrhizal fungal diversity in maize fields by a molecular approach. Biology and Fertility of Soils 48:1-12.
9. Brito, I., M. J. Goss, M. de Carvalho, O. Chatagnier, and D. van Tuinen. 2012. Impact of tillage system on arbuscular mycorrhiza fungal communities in the soil under mediterranean conditions. Soil and Tillage Research 121:63-67.
10. Brussaard, L., P. C. de Ruiter, and G. G. Brown. 2007. Soil biodiversity for agricultural sustainability. Agriculture, Ecosystems and Environment 121:233-244.
11. Bü nemann, E. K., and L. M. Condron. 2007. Phosphorus and sulphur cycling in terrestrial ecosystems. Pages 65-92 in P. Marschner and Z. Rengel, editors. Nutrient cycling in terrestrial ecosystems., Springer, Berlin, Germany.
12. Carlsson, G., and K. Huss-Danell. 2003. Nitrogen fixation in perennial forage legumes in the field. Plant and Soil 253:353-372.
13. Castellanos-Navarrete, A., C. Rodríguez-Aragonés, R. de Goede, M. Kooistra, K. Sayre, L. Brussaard, and M. Pulleman. 2012. Earthworm activity and soil structural changes under conservation agriculture in central Mexico. Soil and Tillage Research 123:61-70.
14. Castillo, C. G., R. Rubio, J. L. Rouanet, and F. Borie. 2006. Early effects of tillage and crop rotation on arbuscular mycorrhizal fungal propagules in an Ultisol. Biology and Fertility of Soils 43:83-92.
15. Chapin, F. S. 1980. The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11:233-260.
16. Cordell, D., J. O. Drangert, and S. White. 2009. The story of phosphorus: global food security and food for thought. Global Environmental Change 19:292-305.
17. Corkidi, L., D. Rowland, N. Johnson, and E. Allen. 2002. Nitrogen fertilization alters the functioning of arbuscular mycorrhizas at two semiarid grasslands. Plant and Soil 240:299-310.
18. Curaqueo, G., J. M. Barea, E. Acevedo, R. Rubio, P. Cornejo, and F. Borie. 2011. Effects of different tillage system on arbuscular mycorrhizal fungal propagules and physical properties in a mediterranean agroecosystem in central Chile. Soil and Tillage Research 113:11-18.
19. de Vries, F. T., et al. 2013. Soil food web properties explain ecosystem services across European land use systems. Proceedings of the National Academy of Sciences USA 110:14296-14301.
20. Douds, D. D., L. Galvez, R. R. Janke, and P. Wagoner. 1995. Effect of tillage and farming system upon populations and distribution of vesicular-arbuscular mycorrhizal fungi. Agriculture, Ecosystems and Environment 52:111-118.
21. Douds, D. D., and P. D. Millner. 1999. Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agriculture, Ecosystems and Environment 74:77-93.
22. Drew, E. A., R. S. Murray, S. E. Smith, and I. Jakobsen. 2003. Beyond the rhizosphere: growth and function of arbuscular mycorrhizal external hyphae in sands of varying pore sizes. Plant and Soil 251:105-114.
23. Feng, Y., A. C. Motta, D. W. Reeves, C. H. Burmester, E. van Santen, and J. A. Osborne. 2003. Soil microbial communities under conventional-till and no-till continuous cotton systems. Soil Biology and Biochemistry 35:1693-1703.
24. Galvez, L., D. D. Douds, L. E. Drinkwater, and P. Wagoner. 2001. Effect of tillage and farming system upon VAM fungus populations and mycorrhizas and nutrient uptake of maize. Plant and Soil 228:299-308.
25. Gavito, M. E., and M. H. Miller. 1998. Early phosphorus nutrition, mycorrhizae development, dry matter partitioning and yield of maize. Plant and Soil 199:177-186.
26. Hart, M. M., and R. J. Reader. 2002. Host plant benefit from association with arbuscular mycorrhizal fungi: variation due to differences in size of mycelium. Biology and Fertility of Soils 36:357-366.
27. Hawksworth, D. L. 2011. Introducing the Draft BioCode (2011). Taxon 60:199-200.
28. Jakobsen, I., L. K. Abbott, and A. D. Robson. 1992a. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytologist 120:371-380.
29. Jakobsen, I., L. K. Abbott, and A. D. Robson. 1992b. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances. New Phytologist 120:509-516.
30. Jansa, J., A. Mozafar, and E. Frossard. 2005. Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant and Soil 276:163-176.
31. Jansa, J., A. Mozafar, G. Kuhn, T. Anken, R. Ruh, I. R. Sanders, and E. Frossard. 2003. Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecological Applications 13:1164-1176.
32. Jansa, J. J., A. M. Mozafar, T. A. Anken, R. R. Ruh, I. S. Sanders, and E. F. Frossard. 2002. Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225-234.
33. Johnson, N. C. 1993. Can fertilization of soil select less mutualistic mycorrhizae? Ecological Applications 3:749-757.
34. Johnson, N. C., J. H. Graham, and F. A. Smith. 1997. Functioning of mycorrhizal associations along the mutualism- parasitism continuum. New Phytologist 135:575-586.
35. Jossi, W., U. Zihlmann, T. Anken, B. Dorn, and M. G. A. van der Heijden. 2011. Reduced tillage protects earthworms. Agrarforschung Schweiz 2:432-439.
36. Kabir, Z. 2005. Tillage or no-tillage: impact on mycorrhizae. Canadian Journal of Plant Science 85:23-29.
37. Kabir, Z., I. P. O'Halloran, J. W. Fyles, and C. Hamel. 1997. Seasonal changes of arbuscular mycorrhizal fungi as affected by tillage practices and fertilization: hyphal density and mycorrhizal root colonization. Plant and Soil 192:285-293.
38. Kabir, Z., I. P. O'Halloran, J. W. Fyles, and C. Hamel. 1998a. Dynamics of the mycorrhizal symbiosis of corn (Zea mays L.): effects of host physiology, tillage practice and fertilization on spatial distribution of extraradical mycorrhizal hyphae in the field. Agriculture, Ecosystems and Environment 68:151-163.
39. Kabir, Z., I. P. O'Halloran, P. Widden, and C. Hamel. 1998b. Vertical distribution of arbuscular mycorrhizal fungi under corn (Zea mays L.) in no-till and conventional tillage systems. Mycorrhiza 8:53-55.
40. Knacker, T., C. A. M. van Gestel, S. E. Jones, A. M. V. M. Soares, H.-J. Schallnas, B. Förster, and C. A. Edwards. 2004. Ring-testing and field-validation of a terrestrial model ecosystem (TME)-an instrument for testing potentially harmful substances: conceptual approach and study design. Ecotoxicology 13:9-27.
41. Koerselman, W., and A. F. M. Meuleman. 1996. The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. Journal of Applied Ecology 33:1441-1450.
42. Lekberg, Y., and R. T. Koide. 2005. Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytologist 168:189-204.
43. Li, X.-L., E. George, and H. Marschner. 1991. Extension of the phosphorus depletion zone in VA-mycorrhizal white clover in a calcareous soil. Plant and Soil 136:41-48.
44. Mathew, R. P., Y. Feng, L. Githinji, R. Ankumah, and K. S. Balkcom. 2012. Impact of no-tillage and conventional tillage systems on soil microbial communities. Applied and Environmental Soil Science 2012:1-10.
45. McGonigle, T. P., and M. H. Miller. 1996. Development of fungi below ground in association with plants growing in disturbed and undisturbed soils. Soil Biology and Biochemistry 28:263-269.
46. McGonigle, T. P., M. H. Miller, D. G. Evans, G. L. Fairchild, and J. A. Swan. 1990. A new method which gives an objective-measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytologist 115:495-501.
47. McGonigle, T. P., K. Yano, and T. Shinhama. 2003. Mycorrhizal phosphorus enhancement of plants in undisturbed soil differs from phosphorus uptake stimulation by arbuscular mycorrhizae over non-mycorrhizal controls. Biology and Fertility of Soils 37:268-273.
48. Miller, M. H., T. P. McGonigle, and H. D. Addy. 1995. Functional ecology of vesicular-arbuscular mycorrhizas as influenced by phosphate fertilization and tillage in an agricultural ecosystem. Critical Reviews in Biotechnology 15:241-255.
49. Miura, F., T. Nakamoto, S. Kaneda, S. Okano, M. Nakajima, and T. Murakami. 2008. Dynamics of soil biota at different depths under two contrasting tillage practices. Soil Biology and Biochemistry 40:406-414.
50. Moora, M., M. Öpik, R. Sen, and M. Zobel. 2004. Native arbuscular mycorrhizal fungal communities differentially influence the seedling performance of rare and common Pulsatilla species. Functional Ecology 18:554-562.
51. Mulder, C., A. Boit, M. Bonkowski, P. C. de Ruiter, G. Mancinelli, M. G. A. van der Heijden, H. J. van Wijnen, J. A. Vonk, and M. Rutgers. 2011. A belowground perspective on Dutch agroecosystems: how soil organisms interact to support ecosystem services. Pages 277-357 in G. Woodward, editor. Advances in ecological research. Elsevier Academic Press, San Diego, California, USA.
52. Nemecek, T., O. Huguenin-Elie, D. Dubois, G. Gaillard, B. Schaller, and A. Chervet. 2011. Life cycle assessment of Swiss farming systems: II. Extensive and intensive production. Agricultural Systems 104:233-245.
53. Nyfeler, D. 2009. Productivity and nitrogen utilisation in productive agricultural grassland: effects of species combinations, species proportions and nitrogen fertilisation. Dissertation. ETH (Swiss Federal Institute of Technology), Zurich, Switzerland.
54. Oehl, F., E. Laczko, A. Bogenrieder, K. Stahr, R. Bösch, M. G. A. van der Heijden, and E. Sieverding. 2010. Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biology and Biochemistry 42:724-738.
55. Oehl, F., E. Sieverding, K. Ineichen, P. Mader, T. Boller, and A. Wiemken. 2003. Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Applied and Environmental Microbiology 69:2816-2824.
56. Oehl, F., E. Sieverding, K. Ineichen, P. Mader, A. Wiemken, and T. Boller. 2009. Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agriculture, Ecosystems and Environment 134:257-268.
57. Oehl, F., E. Sieverding, K. Ineichen, E. A. Ris, T. Boller, and A. Wiemken. 2005. Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytologist 165:273-283.
58. Oehl, F., E. Sieverding, J. Palenzuela, K. Ineichen, and G. Alves da Silva. 2011. Advances in Glomeromycota taxonomy and classification. IMA Fungus 2:191-199.
59. Owusu-Bennoah, E., and B. Mosse. 1979. Plant growth responses to vesicular-arbuscular mycorrhiza. XI. Field inoculation responses in barley, lucerne and onion. New Phytologist 83:671-679.
60. Peigné, J., B. C. Ball, J. Roger-Estrade, and C. David. 2007. Is conservation tillage suitable for organic farming? A review. Soil Use and Management 23:129-144.
61. Pimratch, S., S. Jogloy, N. Vorasoot, B. Toomsan, A. Patanothai, and C. C. Holbrook. 2008. Relationship between biomass production and nitrogen fixation under droughtstress conditions in peanut genotypes with different levels of drought resistance. Journal of Agronomy and Crop Science 194:15-25.
62. Postma-Blaauw, M. B., R. G. M. de Goede, J. Bloem, J. H. Faber, and L. Brussaard. 2010. Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91:460-473.
63. R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
64. Raju, P. S., R. B. Clark, J. R. Ellis, and J. W. Maranville. 1990. Effects of species of VA-mycorrhizal fungi on growth and mineral uptake of sorghum at different temperatures. Plant and Soil 121:165-170.
65. Rosendahl, S., and E. H. Stukenbrock. 2004. Community structure of arbuscular mycorrhizal fungi in undisturbed vegetation revealed by analyses of LSU rDNA sequences. Molecular Ecology 13:3179-3186.
66. Schalamuk, S., S. Velazquez, H. Chidichimo, and M. Cabello. 2006. Fungal spore diversity of arbuscular mycorrhizal fungi associated with spring wheat: effects of tillage. Mycologia 98:16-22.
67. Scheublin, T. R., R. S. P. van Logtestijn, and M. G. A. van der Heijden. 2007. Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species. Journal of Ecology 95:631-638.
68. Schnoor, T., Y. Lekberg, S. Rosendahl, and P. Olsson. 2011. Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza 21:211-220.
69. Scullion, J., W. R. Eason, and E. P. Scott. 1998. The effectivity of arbuscular mycorrhizal fungi from high input conventional and organic grassland and grass-arable rotations. Plant and Soil 204:243-254.
70. Sieverding, E. 1991. Vesicular-arbuscular mycorrhiza management in tropical agrosystems. Deutsche Gesellschaft für Technische Zusammenarbeit, Eschborn, Germany.
71. Smith, F. A., and S. E. Smith. 1996. Mutualism and parasitism: diversity in function and structure in the ''arbuscular'' (VA) mycorrhizal symbiosis. Advances in Botanical Research 22:1-43.
72. Smith, S. E., and D. Read. 2008. Mycorrhizal symbiosis. Third edition. Academic Press, Elsevier, Oxford, UK.
73. Smith, S. E., F. A. Smith, and I. Jakobsen. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133:16-20.
74. Sturny, W. G., A. Chervet, C. Maurer-Troxler, L. Ramseier, M. Müller, R. Schafflü tzel, W. Richner, B. Streit, P. Weisskopf, and U. Zihlmann. 2007. Comparison of no-tillage and conventional plough tillage-a synthesis. Agrarforschung 14:350-357.
75. Sýkorová, Z., K. Ineichen, A. Wiemken, and D. Redecker. 2007. The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza 18:1-14.
76. Tennant, D. 1975. A test of a modified line intersect method of estimating root length. Journal of Ecology 63:995-1001.
77. van der Heijden, M. G. A. 2010. Mycorrhizal fungi reduce nutrient loss from grassland ecosystems. Ecology 91:1163-1171.
78. Verbruggen, E., and E. T. Kiers. 2010. Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evolutionary Applications 3:547-560.
79. Verbruggen, E., E. T. Kiers, P. C. Bakelaar, W. M. Röling, and M. G. A. van der Heijden. 2012. Provision of contrasting ecosystem services by soil communities from different agricultural fields. Plant and Soil 350:43-55.
80. Verbruggen, E., W. F. M. Röling, H. A. Gamper, G. A. Kowalchuk, H. A. Verhoef, and M. G. A. van der Heijden. 2010. Positive effects of organic farming on below-ground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytologist 186:968-979.
81. Vierheilig, H., A. P. Coughlan, U. Wyss, and Y. Piche. 1998. Ink and vinegar, a simple staining technique for arbuscularmycorrhizal fungi. Applied Environmental Microbiology 64:5004-5007.
82. Wagg, C., J. Jansa, B. Schmid, and M. G. A. van der Heijden. 2011. Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecology Letters 14:1001-1009.
83. Watanabe, F. S., and S. R. Olsen. 1965. Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil. Soil Science Society of America Journal 29:677-678.
84. Xavier, L. J. C., and J. J. Germida. 2002. Response of lentil under controlled conditions to co-inoculation with arbuscular mycorrhizal fungi and rhizobia varying in efficacy. Soil Biology and Biochemistry 34:181-188.
85. Yang, A., J. Hu, X. Lin, A. Zhu, J. Wang, J. Dai, and M. Wong. 2012. Arbuscular mycorrhizal fungal community structure and diversity in response to 3-year conservation tillage management in a sandy loam soil in North China. Journal of Soils and Sediments 12:835-843.