Effects of genetically modified, herbicide-tolerant crops and their management on soil food web properties and crop litter decomposition

Journal of Applied Ecology

Volumn 46, Issue 2, 2009, Pages 388-396

  Powell, Jeff R ^a,c   Levy Booth, David J ^a   Gulden, Robert H ^a   Asbil, Wendy L ^a   Campbell, Rachel G ^a   Dunfield, Kari E ^a   Hamill, Allan S ^b   Hart, Miranda M ^a   Lerat, Sylvain ^a   Nurse, Robert E ^b   Pauls, K Peter ^a   Sikkema, Peter H ^a   Swanton, Clarence J ^a   Trevors, Jack T ^a   Klironomos, John N ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Glycine max; Glyphosate; Herbicides; Roundup ready; Soil food web; Transgenic crops; Zea mays

Indexed keywords

ABUNDANCE; AGRICULTURAL ECOSYSTEM; BACTERIUM; BIODIVERSITY; BIOMASS; BIOTECHNOLOGY; CARBON SEQUESTRATION; DETRITIVORY; FIELDWORK; FOOD WEB; GLYPHOSATE; LITTER; MAIZE; MANAGEMENT PRACTICE; MICROCOSM; NUTRIENT CYCLING; PESTICIDE RESISTANCE; SOIL BIOTA; SOIL ECOSYSTEM; SOYBEAN; TRANSGENIC PLANT;

CANADA; NORTH AMERICA; ONTARIO [CANADA];

BACTERIA (MICROORGANISMS); GLYCINE MAX; ZEA MAYS;

EID: 61449185578     PISSN: 00218901     EISSN: 13652664     Source Type: Journal    
DOI: 10.1111/j.1365-2664.2009.01617.x     Document Type: Article

References (63)

1. Allen, M.F. MacMahon, J.A. (1985) Impact of disturbance on cold desert fungi - comparative microscale dispersion patterns. Pedobiologia, 28, 215 224.
2. Anderson, J.R. Slinger, J.M. (1975) Europium chelate and fluorescent brightner staining of soil propagules and their photomicrographic counting. I. Methods. Soil Biology & Biochemistry, 7, 205 209.
3. Annerberg, R. (2003) The present status of the use of geneticallly modified crops in the EU - the current situation and a vision for the future. Acta Agriculturae Scandinavica, Section B - Soil & Plant Science, Suppl. 1, 14 18.
4. Atkinson, D. (1985) The toxicological properties of glyphosate - a summary. The Herbicide Glyphosate (eds E. Grossbard D. Atkinson), pp. 127 133. Butterworth and Co., Ltd, Boston, MA, USA.
5. Bamforth, S.S. (1991) Enumeration of soil ciliate active forms and cysts by a direct count method. Agriculture Ecosystems & Environment, 34, 209 212.
6. Behrens, M.R., Mutlu, N., Chakraborty, S., Dumitru, R., Jiang, W.Z., LaVallee, B.J., Herman, P.L., Clemente, T.E. Weeks, D.P. (2007) Dicamba resistance: enlarging and preserving biotechnology-based weed management strategies. Science, 316, 1185 1188.
7. Berg, M., de Ruiter, P., Didden, W., Janssen, M., Schouten, T. Verhoef, H. (2001) Community food web, decomposition and nitrogen mineralisation in a stratified Scots pine forest soil. Oikos, 94, 130 142.
8. Coleman, D.C., Reid, C.P.P. Cole, C.V. (1983) Biological strategies of nutrient cycling in soil systems. Advances in Ecological Research, 13, 1 55.
9. Cortet, J., Andersen, M.N., Caul, S., Griffiths, B., Joffre, R., Lacroix, B., Sausse, C., Thompson, J. Krogh, P.H. (2006) Decomposition processes under Bt (Bacillus thuringiensis) maize: results of a multi-site experiment. Soil Biology & Biochemistry, 38, 195 199.
10. de Vries, J. Wackernagel, W. (2004) Microbial horizontal gene transfer and the DNA release from transgenic crop plants. Plant and Soil, 266, 91 104.
11. Duke, S.O. (2005) Taking stock of herbicide-resistant crops ten years after introduction. Pest Management Science, 61, 211 218.
12. Dunfield, K.E. Germida, J.J. (2004) Impact of genetically modified crops on soil- and plant-associated microbial communities. Journal of Environmental Quality, 33, 1 10.
13. Eijsackers, H. (1991) Litter fragmentation by isopods as affected by herbicide application. Netherlands Journal of Zoology, 41, 277 303.
14. Faraway, J.J. (2006) Extending the Linear Model with r: Generalized Linear, Mixed Effects and Nonparametric Regression Models. CRC Press, Boca Raton, FL, USA.
15. Feng, P.C.C., Baley, G.J., Clinton, W.P., Bunkers, G.J., Alibhai, M.F., Paulitz, T.C. Kidwell, K.K. (2005) Glyphosate inhibits rust diseases in glyphosate-resistant wheat and soybean. Proceedings of the National Academy of Sciences of the United States of America, 102, 17290 17295.
16. Ferris, H., Bongers, T. de Goede, R.G.M (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Applied Soil Ecology, 18, 13 29.
17. Franz, J.E. (1985) Discovery, development and chemistry of glyphosate. The Herbicide Glyphosate (eds E. Grossbard D. Atkinson), pp. 3 17. Butterworth and Co., Ltd, Boston, MA, USA.
18. Freckman, D.W. Baldwin, J.G. (1990) Nematoda. Soil Biology Guide (ed. D.L. Dindal), pp. 155 200. John Wiley & Sons, Inc., New York.
19. Griffiths, B.S., Caul, S., Thompson, J., Birch, A.N.E., Scrimgeour, C., Cortet, J., Foggo, A., Hackett, C.A. Krogh, P.H. (2006) Soil microbial and faunal community responses to Bt maize and insecticide in two soils. Journal of Environmental Quality, 35, 734 741.
20. Han, S.O. New, P.B. (1994) Effect of water availability on degradation of 2,4-dichlorophenoxyacetic acid (2,4-D) by soil microorganisms. Soil Biology & Biochemistry, 26, 1689 1697.
21. Haughton, A.J., Champion, G.T., Hawes, C., Heard, M.S., Brooks, D.R., Bohan, D.A., Clark, S.J., Dewar, A.M., Firbank, L.G., Osborne, J.L., Perry, J.N., Rothery, P., Roy, D.B., Scott, R.J., Woiwod, I.P., Birchall, C., Skellern, M.P., Walker, J.H., Baker, P., Browne, E.L., Dewar, A.J.G., Garner, B.H., Haylock, L.A., Horne, S.L., Mason, N.S., Sands, R.J.N. Walker, M.J. (2003) Invertebrate responses to the management of genetically modified herbicide-tolerant and conventional spring crops. II. Within-field epigeal and aerial arthropods. Philosophical Transactions of the Royal Society, Series B, 358, 1863 1877.
22. Hawes, C., Haughton, A.J., Osborne, J.L., Roy, D.B., Clark, S.J., Perry, J.N., Rothery, P., Bohan, D.A., Brooks, D.R., Champion, G.T., Dewar, A.M., Heard, M.S., Woiwod, I.P., Daniels, R.E., Young, M.W., Parish, A.M., Scott, R.J., Firbank, L.G. Squire, G.R. (2003) Responses of plants and invertebrate trophic groups to contrasting herbicide regimes in the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. Philosophical Transactions of the Royal Society, Series B, 358, 1899 1913.
23. Hendrix, P.F. Parmelee, R.W. (1985) Decomposition, nutrient loss and microarthropod densities in herbicide-treated grass litter in a Georgia Piedmont USA agroecosystem. Soil Biology & Biochemistry, 17, 421 428.
24. Herrmann, K.M. Weaver, L.M. (1999) The shikimate pathway. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 473 503.
25. Horwitz, W. (2000) Official Methods of Analysis, 17th edn. AOAC International, Gaithersberg, MD, USA.
26. House, G.J., Worsham, A.D., Sheets, T.J. Stinner, R.E. (1987) Herbicide effects on soil arthropod dynamics and wheat straw decomposition in a North Carolina no-tillage agroecosystem. Biology and Fertility of Soils, 4, 109 114.
27. Hunt, G.A. Fogel, R. (1983) Fungal hyphal dynamics in a western Oregon Douglas fir stand. Soil Biology & Biochemistry, 15, 641 649.
28. Hüsken, A. Dietz-Pfeilstetter, A. (2007) Pollen-mediated intraspecific gene flow from herbicide resistant oilseed rape (Brassica napus L.). Transgenic Research, 16, 557 569.
29. James, C. (2007) Global status of commercialized biotech/GM crops: 2007. ISAAA Brief 37-2007: Executive Summary. Ithaca, NY. http://www.isaaa.org/ resources/publications/briefs/37/executivesummary/default.html (last accessed 22 July 2008).
30. Janssen, M.P.M. Heijmans, G. (1998) Dynamics and stratification of protozoa in the organic layer of a Scots pine forest. Biology and Fertility Of Soils, 26, 285 292.
31. Kimpinski, J. (1993) Nematodes. Soil Sampling & Methods of Analysis (ed. M.R. Carter pp. 333 350. Lewis Publishers, Boca Raton, FL, USA.
32. Kjøller, A. Struwe, S. (1982) Microfungi in ecosystems: fungal occurrence and activity in litter and soil. Oikos, 39, 391 422.
33. Levy-Booth, D.J., Campbell, R.G., Gulden, R.H., Hart, M.M., Powell, J.R., Klironomos, J.N., Pauls, K.P., Swanton, C.J., Trevors, J.T. Dunfield, K.E. (2007) Cycling of extracellular DNA in the soil environment, Soil Biology and Biochemistry, 39, 2977 2991.
34. Lilley, A.K., Bailey, M.J., Cartwright, C., Turner, S.L. Hirsch, P.R. (2006) Life on Earth: the impact of GM plants on soil ecology? Trends in Biotechnology, 24, 9 14.
35. Liphadzi, K.B., Al-Khatib, K., Bensch, C.N., Stahlman, P.W., Dille, J.A., Todd, T., Rice, C.W., Horak, M.J. Head, G. (2005) Soil microbial and nematode communities as affected by glyphosate and tillage practices in a glyphosate-resistant cropping system. Weed Science, 53, 536 545.
36. Lussenhop, J. (1971) A simplified canister-type soil arthropod extractor. Pedobiologia, 11, 40 45.
37. Malkomes, H.P. (1992) Herbicide effects on microbial activity in the soil under varied ecological conditions - influence of soil moisture. Weed Research, 32, 221 230.
38. Marra, M.C., Piggott, N.E. Carlson, G.A. (2004) The net benefits, including convenience, of Roundup Ready soybeans: results from a national survey. Technical Bulletin 2004-3. NSF Center for IPM, Raleigh, NC, USA.
39. Moore, J.C., McCann, K. de Ruiter, P.C. (2005) Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. Pedobiologia, 49, 499 510.
40. Morandin, L.A. Winston, M.L. (2005) Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecological Applications, 15, 871 881.
41. Morris, S.J., Zink, T., Conners, K. Allen, M.F. (1997) Comparison between fluorescein diacetate and differential fluorescent staining procedures for determining fungal biomass in soils. Applied Soil Ecology, 6, 161 167.
42. NASS (2008) Acreage. US Department of Agriculture, National Agricultural Statistics Service, Washington, DC.
43. OMAFRA (2006) Publication 75, Guide to Weed Control. Queen's Printer for Ontario, Guelph, ON, Canada.
44. Owen, M.D.K. (2008) Weed species shifts in glyphosate-resistant crops. Pest Management Science, 64, 377 387.
45. Pidgeon, J.D, May, M.J, Perry, J.N. Poppy, G.M. (2007) Mitigation of indirect environmental effects of GM crops. Proceedings of the Royal Society, Series B, 274, 1475 1479.
46. Pinheiro, J., Bates, D., DebRoy, S. Sarkar, D. (2006) Nlme: linear and nonlinear mixed effects models. rpackage version 3·1-78. r Foundation for Statistical Computing, Vienna, Austria.
47. Pinheiro, J.C. Bates, D.M. (2000) Mixed-Effects Models in S and S-Plus. Springer Verlag, New York.
48. Powell, J.R. Dunfield, K.E. (2007) Non-target impacts of genetically-modified, herbicide-resistant crops on soil microbial and faunal communities. The First Decade of Herbicide Resistant Crops in Canada (eds R.H. Gulden C.J. Swanton), pp. 127 137. Canadian Weed Science Society, Sainte Anne de Bellevue, QC, Canada.
49. Powell, J.R., Gulden, R.H., Hart, M.M., Campbell, R.G., Levy-Booth, D.J., Dunfield, K.E., Pauls, K.P., Swanton, C.J., Trevors, J.T. Klironomos, J.N. (2007) Mycorrhizal and rhizobial colonization of genetically modified and conventional soybeans. Applied and Environmental Microbiology, 73, 4365 4367.
50. R Development Core Team (2006) r: A Language and Environment for Statistical Computing. Version 2·3. r Foundation for Statistical Computing, Vienna, Austria.
51. Roberts, F., Roberts, C.W., Johnson, J.J., Kyle, D.E., Krell, T., Coggins, J.R., Coombs, G.H., Milhous, W.K., Tzipori, S., Ferguson, D.J.P., Chakrabarti, D. McLeod, R. (1998) Evidence for the shikimate pathway in apicomplexan parasites. Nature, 393, 801 805.
52. Rooney, N., McCann, K., Gellner, G. Moore, J.C. (2006) Structural asymmetry and the stability of diverse food webs. Nature, 442, 265 269.
53. Saxena, D. Stotzky, G. (2001) Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biology & Biochemistry, 33, 1225 1230.
54. Seppanen, S.K., Pasonen, H.L., Vauramo, S., Vahala, J., Toikka, M., Kilpelainen, I., Setala, H., Teeri, T.H., Timonen, S. Pappinen, A. (2007) Decomposition of the leaf litter and mycorrhiza forming ability of silver birch with a genetically modified lignin biosynthesis pathway. Applied Soil Ecology, 36, 100 106.
55. Swift, M.J., Cook, A.G. Perfect, T.J. (1979) Decomposition in Terrestrial Ecosystems. Blackwell Scientific Publication, Oxford, UK.
56. Tilston, E.L., Halpin, C. Hopkins, D.W. (2004) Genetic modifications to lignin biosynthesis in field-grown poplar trees have inconsistent effects on the rate of woody trunk decomposition. Soil Biology & Biochemistry, 36, 1903 1906.
57. Tueben, A. (1991) Nutrient availability and interactions between soil arthropods and microorganisms during decomposition of coniferous litter: a mesocosm study. Biology and Fertility of Soils, 10, 256 266.
58. Van Veen, J.A. Paul, E.A. (1979) Conversion of biovolume measurements of soil organisms grown under various moisture tensions to biomass and their nutrient content. Applied and Environmental Microbiology, 37, 686 692.
59. Vauramo, S., Pasonen, H.L., Pappinen, A. Setala, H. (2006) Decomposition of leaf litter from chitinase transgenic silver birch (Betula pendula) and effects on decomposer populations in a field trial. Applied Soil Ecology, 32, 338 349.
60. Wardle, D.A. (2002) Communities and Ecosystems: Linking the Aboveground and Belowground Components. Princeton University Press, Princeton, NJ, USA.
61. Wardle, D.A. Parkinson, D. (1992) The influence of the herbicide glyphosate on interspecific interactions between four soil fungal species. Mycological Research, 96, 180 186.
62. Westra, P., Wilson, R.G., Miller, S.D., Stahlman, P.W., Wicks, G.W., Chapman, P.L., Withrow, J., Legg, D., Alford, C. Gaines, T.A. (2008) Weed population dynamics after six years under glyphosate- and conventional herbicide-based weed control strategies. Crop Science, 48, 1170 1177.
63. Zablotowicz, R.M. Reddy, K.N. (2004) Impact of glyphosate on the Bradyrhizobium japonicum symbiosis with glyphosate-resistant transgenic soybean: a minireview. Journal of Environmental Quality, 33, 825 831.