Response of Nitrous Oxide Flux to Addition of Anecic Earthworms to an Agricultural Field


The burrowing and feeding activities of earthworms may have a strong effect on the flux of N2O from agricultural soils. As such, shifts to agricultural management practices that increase the number of earthworms require an understanding of the role of earthworms in N2O dynamics. We conducted a field experiment to examine the effects of addition of anecic earthworms (Lumbricus terrestris) on N2O flux in a field previously planted with corn (Zea mays) in southern Rhode Island, USA. Plots were amended with (15NH4)2SO4 and either 0 (CTL) or 48 L. terrestris m-2 (EW). The flux of N2O, 15N2O and 15N2 was measured over 28 days between October and November 2008. The EW treatment had a significantly higher flux of N2O and 15N2O 1 - 3 days after 15NH4 addition. No treatment effects were observed on 15N2 flux. The addition of earthworms significantly increased (Day 1) and decreased (Day 12) the mole fraction of N2O relative to the CTL. Our results suggest that anecic earthworm additions can increase N2O flux from inorganic fertilizer N amendments, but the effects appear to short-lived.

Share and Cite:

J. Amador and E. Avizinis, "Response of Nitrous Oxide Flux to Addition of Anecic Earthworms to an Agricultural Field," Open Journal of Soil Science, Vol. 3 No. 2, 2013, pp. 100-106. doi: 10.4236/ojss.2013.32011.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] J. P. Schimel and E. A. Holland, “Global Gases,” In: J. J. Fuhrman, D. M. Sylvia, P. G. Hartel and D. A. Zuberer, Eds., Principles and Applications of Soil Microbiology, 2nd Edition, Pearson-Prentice Hall, Upper Saddle River, 2005, pp. 491-509.
[2] C. A. Edwards, “The Importance of Earthworms as Key Representatives of the Soil Fauna,” In: C. A. Edwards, Ed., Earthworm Ecology, 2nd Edition, CRC Press, Boca Raton, 2004, pp. 3-11. doi:10.1201/9781420039719.pt1
[3] M. K. Firestone, R. B. Firestone and J. M. Tiedje, “Nitrous Oxide from Soil Denitrification: Factors Controlling Its Biological Production,” Science, Vol. 208, 1980, pp. 749-751. doi:10.1126/science.208.4445.749
[4] A. J. Tugel and A. M. Lewandowski, “Soil Biology Primer,” NRCS Soil Quality Institute, Ames, 1999.
[5] FAO (Food and Agriculture Organization of the United Nations), “Manual on Integrated Soil Management and Conservation Practices,” No. 8, Rome, 2000.
[6] C. Sandretto, “Conservation Tillage Firmly Planted in U.S. Agriculture,” Agricultural Outlook: Economic Research Service—USDA, 2001, pp. 5-6.
[7] J. M. Holland, “The Environmental Consequences of Adopting Conservation Tillage in Europe: Reviewing the Evidence,” Agriculture, Ecosystems & Environment, Vol. 103, No. 1, 2004, pp. 1-25. doi:10.1016/j.agee.2003.12.018
[8] R. Fowler and J. Rockstrom, “Conservation Tillage for Sustainable Agriculture: An Agrarian Revolution Gathers Momentum in Africa,” Soil and Tillage Research, Vol. 61, No. 1-2, 2001, pp. 93-107. doi:10.1016/S0167-1987(01)00181-7
[9] E. G. Gregorich, P. Rochette, A. J. VandenBygaart and D. A. Angers, “Greenhouse Gas Contributions of Agricultural Soils and Potential Mitigation Practices in Eastern Canada,” Soil and Tillage Research, Vol. 83, No. 1, 2005, pp. 53-72. doi:10.1016/j.still.2005.02.009
[10] R. Lal, J. M. Kimble, R. F. Follett and C. B. Cole, “The Potential of U.S. Cropland to Sequester Carbon and Mitigate the Greenhouse Effect,” CRC Press, Boca Raton, 1998.
[11] C. A. Edwards and J.R. Lofty, “The Effect of Direct Drilling and Minimal Cultivation on Earthworm Populations,” Journal of Applied Ecology, Vol. 19, 1982, pp. 723-734. doi:10.2307/2403277
[12] W. Ehlers, “Observations on Earthworm Channels and Infiltration on Tilled and Untilled Loess Soil,” Soil Science, Vol. 119, 1975, pp. 242-249. doi:10.1097/00010694-197503000-00010
[13] W. M. Edwards, M. J. Shipitalo, L. B. Owens and L. D. Norton, “Effect of Lumbricus terrestris L. Burrows on Hydrology of Continuous No-Till Corn Fields,” Geo derma, Vol. 46, No. 1-3, 1990, pp. 73-84. doi:10.1016/0016-7061(90)90008-W
[14] V. Nuutinen, “Earthworm Community Response to Tillage and Residue Management on Different Soil Types in Southern Finland,” Soil and Tillage Research, Vol. 23, No. 3, 1992, pp. 221-239. doi:10.1016/0167-1987(92)90102-H
[15] C. A. Edwards, “Can Earthworms Harm the Planet?” Bio Cycle, Vol. 49, 2008, p. 53.
[16] J. G. Ehrenfeld, “Ecosystem Consequences of Biological Invasions,” Annual Review of Ecology, Evolution, and Systematics, Vol. 41, 2010, pp. 59-80. doi:10.1146/annurev-ecolsys-102209-144650
[17] E. Rizhiya, C. Bertora, P. C. J. van Vliet, P. J. Kuikman, J. H. Faber and J. W. van Groenigen, “Earthworm Activity as a Determinant for N2O Emission From Crop Residue,” Soil Biology & Biochemistry, Vol. 39, No. 8, 2007, pp. 2058-2069. doi:10.1016/j.soilbio.2007.03.008
[18] C. Bertora, P. C. J. van Vliet, E. W. J. Hummelink and J. W. van Groenigen, “Do Earthworms Increase N2O Emissions in Ploughed Grassland?” Soil Biology & Biochemistry, Vol. 39, No. 2, 2007, pp. 632-640. doi:10.1016/j.soilbio.2006.09.015
[19] A. K. Evers, T. A. Demers, A. M. Gordon and N. V. Thevathasan, “The Effects of Earthworm (Lumbricus terrestris L.) Population Density and Soil Water Content Interactions on Nitrous Oxide Emissions from Agricultural Soils,” Applied and Environmental Soil Science, Vol. 2010, 2010, Article ID: 737096, 9 p. doi:10.1155/2010/737096
[20] G. Giannopoulos, M. M. Pulleman and J. W. Van Groenigen, “Interactions netween Residue Placement and Earthworm Ecological Strategy Affect Aggregate Turn over and N2O Dynamics in Agricultural Soil,” Soil Bio logy & Biochemistry, Vol. 42, No. 4, 2010, pp. 618-625. doi:10.1016/j.soilbio.2009.12.015
[21] J. A. Amador and J. H. Gorres, “Role of the Anecic Earthworm Lumbricus terrestris L. in the Distribution of Plant Residue Nitrogen in a Corn (Zeamays)—Soil System,” Applied Soil Ecology, Vol. 30, No. 3, 2005, pp. 203-214. doi:10.1016/j.apsoil.2005.02.011
[22] Soil Survey Staff, “Official Soil Series Descriptions.”
[23] A. R. Mosier and D. S. Schimel, “Nitrification and Denitrification,” In: R. Knowles and T. H. Blackburn, Eds., Nitrogen Isotope Techniques, Academic Press, San Diego, 1993, pp. 181-208.
[24] M. C. Savin, J. H. Gorres, D. A. Neher and J. A. Amador, “Biogeophysical Factors Influencing Soil Respiration and Mineral Nitrogen Content in an Old Field Soil,” Soil Biology & Biochemistry, Vol. 33, No. 4-5, 2001, pp. 429-438. doi:10.1016/S0038-0717(00)00182-6
[25] P. M. Groffman and J. M. Tiedje, “Denitrification Hysteresis during Wetting and Drying Cycles in Soil,” Soil Science Society of America Journal, Vol. 52, 1988, pp. 1626-1629. doi:10.2136/sssaj1988.03615995005200060022x
[26] T. B. Parkin and E. C. Berry, “Microbial Nitrogen Trans formations in Earthworm Burrows,” Soil Biology & Bio chemistry, Vol. 31, No. 13, 1999, pp. 1765-1771. doi:10.1016/S0038-0717(99)00085-1
[27] T. B. Parkin and E. C. Berry, “Nitrogen Transformations Associated with Earthworm Casts,” Soil Biology & Bio chemistry, Vol. 26, No. 9, 1994, pp. 1233-1238. doi:10.1016/0038-0717(94)90148-1
[28] W. Borken, S. Gründel and F. Beese, “Potential Contribution of Lumbricus terrestris L. to Carbon Dioxide, Methane and Nitrous Oxide Fluxes from a Forest Soil,” Biology and Fertility of Soils, Vol. 32, No. 2, 2000, pp. 142-148. doi:10.1007/s003740000228
[29] A. B. Speratti and J. K. Whalen, “Carbon Dioxide and Nitrous Oxide Fluxes from Soil as Influenced by Anecic and Endogeic Earthworms,” Applied Soil Ecology, Vol. 38, No. 1, 2008, pp. 27-33. doi:10.1016/j.apsoil.2007.08.009
[30] P. K. Wust, M. A. Horn, G. Henderson, P. H. Janssen, B. H. A. Rehm and H. L. Drake, “Gut-Associated Denitrification and in Vivo Emission of Nitrous Oxide by the Earthworm Families Megascolecidae and Lumbricidae in New Zealand,” Applied and Environmental Microbiology, Vol. 75, No. 11, 2009, pp. 3430-3436. doi:10.1128/AEM.00304-09
[31] H. L. Drake and M. A. Horn, “Earthworms as a Transient Heaven for Terrestrial Denitrifying Microbes: A Re view,” Engineering in Life Sciences, Vol. 6, No. 3, 2006, pp. 261-265. doi:10.1002/elsc.200620126
[32] R. N. van den Heuvel, M. M. Hefting, N. C. G. Tan, M. S. M. Jetten and J. T. A. Verhoeven, “N2O Emission Hot spots at Different Spatial Scales and Governing Factors for Small Scale Hotspots,” Science of the Total Environment, Vol. 407, No. 7, 2009, pp. 2325-2332. doi:10.1016/j.scitotenv.2008.11.010
[33] M. A. Cavigelli and G. P. Robertson, “Role of Denitrifier Diversity in Rates of Nitrous Oxide Consumption in a Terrestrial Ecosystem,” Soil Biology & Biochemistry, Vol. 33, No. 3, 2001, pp. 297-310. doi:10.1016/S0038-0717(00)00141-3
[34] J. H. Gorres, M. C. Savin and J. A. Amador, “Dynamics of Carbon and Nitrogen Mineralization, Microbial Bio mass, and Nematode Abundance Within and Outside the Burrow Walls of Anecic Earthworms (Lumbricus terrestris),” Soil Science, Vol. 162, 1997, pp. 666-671. doi:10.1097/00010694-199709000-00008
[35] A. Kretzschmar and P. Monestiez, “Physical Control of Soil Biological Activity Due to Endogeic Earthworm Behavior,” Soil Biology & Biochemistry, Vol. 24, No. 12, 1992, pp. 1609-1614. doi:10.1016/0038-0717(92)90158-T
[36] J. H. G?rres, M. C. Savin and J. A. Amador, “Soil Micropore Structure and Carbon Mineralization in Burrows and Casts of an Anecic Earthworm (Lumbricus terrestris),” Soil Biology & Biochemistry, Vol. 33, No. 14, 2001, pp. 1881-1887. doi:10.1016/S0038-0717(01)00068-2

Copyright © 2022 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.