Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Greenhouse-gas emissions from soils increased by earthworms

Abstract

Earthworms play an essential part in determining the greenhouse-gas balance of soils worldwide, and their influence is expected to grow over the next decades. They are thought to stimulate carbon sequestration in soil aggregates, but also to increase emissions of the main greenhouse gases carbon dioxide and nitrous oxide. Hence, it remains highly controversial whether earthworms predominantly affect soils to act as a net source or sink of greenhouse gases. Here, we provide a quantitative review of the overall effect of earthworms on the soil greenhouse-gas balance. Our results suggest that although earthworms are largely beneficial to soil fertility, they increase net soil greenhouse-gas emissions.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Percentage effect of earthworm presence on N2O and CO2 emissions from soil and SOC.
Figure 2: Percentage effect of earthworm presence on the net GWP of the soil for each observation that included both N2O and CO2 flux measurements and the average for all observations.

References

  1. Rastogi, M., Singh, S. & Pathak, H. Emission of carbon dioxide from soil. Curr. Sci. 82, 510–518 (2002).

    CAS  Google Scholar 

  2. Smith, K. A. et al. Exchange of greenhouse gases between soil and atmosphere: Interactions of soil physical factors and biological processes. Eur. J. Soil Sci. 54, 779–791 (2003).

    Article  Google Scholar 

  3. Le Mer, J. & Roger, P. Production, oxidation, emission and consumption of methane by soils: A review. Eur. J. Soil Biol. 37, 25–50 (2001).

    Article  CAS  Google Scholar 

  4. Wrage, N., Velthof, G. L., van Beusichem, M. L. & Oenema, O. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol. Biochem. 33, 1723–1732 (2001).

    Article  CAS  Google Scholar 

  5. Kool, D. M. et al. Nitrifier denitrification can be a source of N2O from soil: A revised approach to the dual-isotope labelling method. Eur. J. Soil Sci. 61, 759–772 (2010).

    Article  CAS  Google Scholar 

  6. Brown, G. G., Barois, I. & Lavelle, P. Regulation of soil organic matter dynamics and microbial activityin the drilosphere and the role of interactions with other edaphic functional domains. Eur. J. Soil Biol. 36, 177–198 (2000).

    Article  Google Scholar 

  7. Lavelle, P. et al. Soil function in a changing world: The role of invertebrate ecosystem engineers. Eur. J. Soil Biol. 33, 159–193 (1997).

    CAS  Google Scholar 

  8. Edwards, C. A. Earthworm Ecology 2nd edn (CRC, 2004).

    Book  Google Scholar 

  9. Drake, H. L. & Horn, M. A. Earthworms as a transient heaven for terrestrial denitrifying microbes: A review. Eng. Life Sci. 6, 261–265 (2006). Emission of nitrogenous gases (N 2 O and N 2 ) appears to be primarily produced by soil-derived denitrifying bacteria when they are subjected to the unique in situ conditions of the earthworm gut; the particular microenvironment of the earthworm gut might also affect the fitness and diversity of certain members of the soil microbial biome.

    Article  CAS  Google Scholar 

  10. Elliott, P. W., Knight, D. & Anderson, J. M. Variables controlling denitrification from earthworm casts and soil in permanent pastures. Biol. Fert. Soils 11, 24–29 (1991).

    Article  CAS  Google Scholar 

  11. Chapuis-Lardy, L. et al. Effect of the endogeic earthworm Pontoscolex corethrurus on the microbial structure and activity related to CO2 and N2O fluxes from a tropical soil (Madagascar). Appl. Soil Ecol. 45, 201–208 (2010). The presence of P. corethrurus induced a significant increase in CO 2 emissions, but did not affect N 2 O fluxes when measured at mesocosm level, thereby showing opposing effects of earthworms on CO 2 and N 2 O emissions within the same study.

    Article  Google Scholar 

  12. Giannopoulos, G., Pulleman, M. M. & van Groenigen, J. W. Interactions between residue placement and earthworm ecological strategy affect aggregate turnover and N2O dynamics in agricultural soil. Soil Biol. Biochem. 42, 618–625 (2010). Earthworm-induced N 2 O emissions reflect earthworm feeding strategies: epigeic earthworms can increase N 2 O emissions when residue is applied on the surface; endogeic earthworms when residue is incorporated into the soil by humans (tillage) or by other earthworm species. The relationships between (functional) soil biodiversity and the soil greenhouse-gas balance are important but intricate.

    Article  CAS  Google Scholar 

  13. Lubbers, I. M., Brussaard, L., Otten, W. & van Groenigen, J. W. Earthworm-induced N mineralization in fertilized grassland increases both N2O emission and crop-N uptake. Eur. J. Soil Sci. 62, 152–161 (2011).

    Article  CAS  Google Scholar 

  14. Rizhiya, E. et al. Earthworm activity as a determinant for N2O emission from crop residue. Soil Biol. Biochem. 39, 2058–2069 (2007).

    Article  CAS  Google Scholar 

  15. Lavelle, P. et al. in Earthworm Ecology (ed. Edwards, C. A.) 145–160 (CRC, 2004).

    Google Scholar 

  16. Bossuyt, H., Six, J. & Hendrix, P. F. Protection of soil carbon by microaggregates within earthworm casts. Soil Biol. Biochem. 37, 251–258 (2005).

    Article  CAS  Google Scholar 

  17. Pulleman, M. M., Six, J., van Breemen, N. & Jongmans, A. G. Soil organic matter distribution and microaggregate characteristics as affected by agricultural management and earthworm activity. Eur. J. Soil Sci. 56, 453–467 (2005).

    Article  CAS  Google Scholar 

  18. Six, J., Bossuyt, H., Degryze, S. & Denef, K. A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Till. Res. 79, 7–31 (2004). The quantification of aggregate formation and SOM stabilization can greatly benefit from viewing aggregates as dynamic rather than static entities; the activity of earthworms has a decisive role in the formation of macro- and microaggregates.

    Article  Google Scholar 

  19. Hendrix, P. F. & Bohlen, P. J. Exotic earthworm invasions in North America: Ecological and policy implications. Bioscience 52, 801–811 (2002). Invasions of exotic earthworms in North America can have negative implications for soil processes, other animals and plant species. More basic knowledge is needed of the natural history and ecology of invasive earthworms in their native habitats, and in ecosystems where they have invaded and had significant impacts.

    Article  Google Scholar 

  20. Norse, D. & Tschirley, J. in World Agriculture: Towards 2015/2030. An FAO Perspective (ed. Bruinsma, J.) 331–355 (Food and Agriculture Organization, 2003).

    Google Scholar 

  21. Hobbs, P. R., Sayre, K. & Gupta, R. The role of conservation agriculture in sustainable agriculture. Phil. Trans. R. Soc. Lond. B 363, 543–555 (2008).

    Article  Google Scholar 

  22. Chan, K. Y. An overview of some tillage impacts on earthworm population abundance and diversity — Implications for functioning of soils. Soil Till. Res. 57, 179–191 (2001).

    Article  Google Scholar 

  23. Decaëns, T. & Jiménez, J. J. Earthworm communities under an agricultural intensification gradient in Colombia. Plant Soil 240, 133–143 (2002).

    Article  Google Scholar 

  24. Bradley, R. L., Chroňáková, A., Elhottová, D. & Šimek, M. Interactions between land-use history and earthworms control gross rates of soil methane production in an overwintering pasture. Soil Biol. Biochem. 53, 64–71 (2012).

    Article  CAS  Google Scholar 

  25. Contreras-Ramos, S. M., Alvarez-Bernal, D., Montes-Molina, J. A., van Cleemput, O. & Dendooven, L. Emission of nitrous oxide from hydrocarbon contaminated soil amended with waste water sludge and earthworms. Appl. Soil Ecol. 41, 69–76 (2009).

    Article  Google Scholar 

  26. Speratti, A. B. & Whalen, J. K. Carbon dioxide and nitrous oxide fluxes from soil as influenced by anecic and endogeic earthworms. Appl. Soil Ecol. 38, 27–33 (2008). After an experimental period of 28 days, earthworms were responsible for 7–58% of the total CO 2 flux from soil, compared to the control (no earthworms), but did not affect the N 2 O flux. Species-specific stimulation of nitrifiers and denitrifiers may be related to unique structures (casts, burrows) produced by L. terrestris and A. caliginosa , but this remains to be confirm ed.

    Article  Google Scholar 

  27. Binet, F. et al. Significance of earthworms in stimulating soil microbial activity. Biol. Fert. Soils 27, 79–84 (1998).

    Article  Google Scholar 

  28. Butenschoen, O., Ji, R., Schaffer, A. & Scheu, S. The fate of catechol in soil as affected by earthworms and clay. Soil Biol. Biochem. 41, 330–339 (2009).

    Article  CAS  Google Scholar 

  29. Hedde, M., Bureau, F., Akpa-Vinceslas, M., Aubert, M. & Decaëns, T. Beech leaf degradation in laboratory experiments: Effects of eight detritivorous invertebrate species. Appl. Soil Ecol. 35, 291–301 (2007).

    Article  Google Scholar 

  30. Martin, A. Short- and long-term effects of the endogeic earthworm Millsonia anomala (Omodeo) (Megascolecidæ, Oligochæta) of tropical savannas, on soil organic matter. Biol. Fert. Soils 11, 234–238 (1991).

    Article  Google Scholar 

  31. Fragoso, C. et al. Agricultural intensification, soil biodiversity and agroecosystem function in the tropics: The role of earthworms. Appl. Soil Ecol. 6, 17–35 (1997).

    Article  Google Scholar 

  32. Velthof, G., Kuikman, P. & Oenema, O. Nitrous oxide emission from soils amended with crop residues. Nutr. Cycl. Agroecosyst. 62, 249–261 (2002).

    Article  CAS  Google Scholar 

  33. Nebert, L. D., Bloem, J., Lubbers, I. M. & van Groenigen, J. W. Association of earthworm-denitrifier interactions with increased emissions of nitrous oxide from soil mesocosms amended with crop residue. Appl. Environ. Microbiol. 77, 4097–4104 (2011).

    Article  CAS  Google Scholar 

  34. Fonte, S. J. & Six, J. Earthworms and litter management contributions to ecosystem services in a tropical agroforestry system. Ecol. Appl. 20, 1061–1073 (2010).

    Article  Google Scholar 

  35. Cortez, J. & Bouche, M. B. Do earthworms eat living roots? Soil Biol. Biochem. 24, 913–915 (1992).

    Article  Google Scholar 

  36. Scheu, S. Effects of earthworms on plant growth: Patterns and perspectives: The 7th international symposium on earthworm ecology. Pedobiologia 47, 846–856 (2003).

    Google Scholar 

  37. Brown, G. et al. in Earthworm Management in Tropical Agroecosystems (eds Lavelle, P., Brussaard, L. & Hendrix, P. F.) 87–147 (CAB International, 1999).

    Google Scholar 

  38. Eisenhauer, N. & Scheu, S. Earthworms as drivers of the competition between grasses and legumes. Soil Biol. Biochem. 40, 2650–2659 (2008).

    Article  CAS  Google Scholar 

  39. Laossi, K-R. et al. Effects of an endogeic and an anecic earthworm on the competition between four annual plants and their relative fecundity. Soil Biol. Biochem. 41, 1668–1673 (2009).

    Article  CAS  Google Scholar 

  40. Barot, S., Ugolini, A. & Brikci, F. B. Nutrient cycling efficiency explains the long-term effect of ecosystem engineers on primary production. Funct. Ecol. 21, 1–10 (2007).

    Article  Google Scholar 

  41. Laossi, K.-R., Noguera, D. C., Decäens, T. & Barot, S. The effects of earthworms on the demography of annual plant assemblages in a long-term mesocosm experiment. Pedobiologia 54, 127–132 (2011).

    Article  Google Scholar 

  42. Burtelow, A. E., Bohlen, P. J. & Groffman, P. M. Influence of exotic earthworm invasion on soil organic matter, microbial biomass and denitrification potential in forest soils of the northeastern United States. Appl. Soil Ecol. 9, 197–202 (1998).

    Article  Google Scholar 

  43. Marhan, S., Langel, R., Kandeler, E. & Scheu, S. Use of stable isotopes (13C) for studying the mobilisation of old soil organic carbon by endogeic earthworms (Lumbricidae). Eur. J. Soil Biol. 43, S201–S208 (2007).

    Article  CAS  Google Scholar 

  44. Curry, J. P. & Schmidt, O. The feeding ecology of earthworms — A review. Pedobiologia 50, 463–477 (2007).

    Article  Google Scholar 

  45. Frelich, L. E. et al. Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol. Invasions 8, 1235–1245 (2006).

    Article  Google Scholar 

  46. Crooks, J. A. Characterizing ecosystem-level consequences of biological invasions: The role of ecosystem engineers. Oikos 97, 153–166 (2002).

    Article  Google Scholar 

  47. Hale, C., Frelich, L., Reich, P. & Pastor, J. Effects of European earthworm invasion on soil characteristics in northern hardwood forests of Minnesota, USA. Ecosystems 8, 911–927 (2005).

    Article  CAS  Google Scholar 

  48. Tylianakis, J. M., Didham, R. K., Bascompte, J. & Wardle, D. A. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363 (2008).

    Article  Google Scholar 

  49. Timmerman, A., Bos, D., Ouwehand, J. & de Goede, R. G. M. Long-term effects of fertilisation regime on earthworm abundance in a semi-natural grassland area. Pedobiologia 50, 427–432 (2006).

    Article  Google Scholar 

  50. Borken, W., Grundel, S. & Beese, F. Potential contribution of Lumbricus terrestris L. to carbon dioxide, methane and nitrous oxide fluxes from a forest soil. Biol. Fert. Soils 32, 142–148 (2000).

    Article  CAS  Google Scholar 

  51. Hedges, L. V. & Olkin, I. Statistical Methods for Meta-analysis (Academic, 1985).

    Google Scholar 

  52. Rosenberg, M. S. B., Adams, D. C. & Gurevitch, J. Metawin: Statistical Software for Meta-Analysis Version 2.0. (Sinauer Associates, 2000).

    Google Scholar 

  53. Tianxiang, L., Huixin, L., Tong, W. & Feng, H. Influence of nematodes and earthworms on the emissions of soil trace gases (CO2, N2O). Acta Ecol. Sin. 28, 993–999 (2008).

    Article  Google Scholar 

  54. Speratti, A., Whalen, J. & Rochette, P. Earthworm influence on carbon dioxide and nitrous oxide fluxes from an unfertilized corn agroecosystem. Biol. Fert. Soils 44, 405–409 (2007).

    Article  Google Scholar 

  55. Marhan, S., Rempt, F., Hogy, P., Fangmeier, A. & Kandeler, E. Effects of Aporrectodea caliginosa (Savigny) on nitrogen mobilization and decomposition of elevated CO2 Charlock mustard litter. J. Plant Nutr. Soil Sci. 173, 861–868 (2010).

    Article  CAS  Google Scholar 

  56. Bertora, C., van Vliet, P. C. J., Hummelink, E. W. J. & van Groenigen, J. W. Do earthworms increase N2O emissions in ploughed grassland? Soil Biol. Biochem. 39, 632–640 (2007).

    Article  CAS  Google Scholar 

  57. Janzen, H. H. The soil carbon dilemma: Shall we hoard it or use it? Soil Biol. Biochem. 38, 419–424 (2006). In his 'Points of view', Janzen considers ways to increase C inputs to soil; seeking to optimize the timing of decay; and to gain a better understanding — from an ecosystem perspective — of the flows of C, rather than just the stocks. He suggests that now, when we aim to regain some of the C lost, we may need new ways of thinking about soil C dynamics, and tuning them for the services expected of our ecosystems.

    Article  CAS  Google Scholar 

  58. Barois, I., Villemin, G., Lavelle, P. & Toutain, F. Transformation of the soil structure through Pontoscolex corethrurus (Oligochaeta) intestinal tract. Geoderma 56, 57–66 (1993).

    Article  Google Scholar 

  59. Jongmans, A. G., Pulleman, M. M. & Marinissen, J. C. Y. Soil structure and earthworm activity in a marine silt loam under pasture versus arable land. Biol. Fert. Soils 33, 279–285 (2001).

    Article  CAS  Google Scholar 

  60. Pulleman, M. M., Six, J., Uyl, A., Marinissen, J. C. Y. & Jongmans, A. G. Earthworms and management affect organic matter incorporation and microaggregate formation in agricultural soils. Appl. Soil Ecol. 29, 1–15 (2005).

    Article  Google Scholar 

  61. Ruz-Jerez, B. E., Ball, P. R. & Tillman, R. W. Laboratory assessment of nutrient release from a pasture soil receiving grass or clover residues, in the presence or absence of Lumbricus rubellus or Eisenia fetida. Soil Biol. Biochem. 24, 1529–1534 (1992).

    Article  Google Scholar 

  62. Bouché, M. B. Strategies lombriciennes. Ecol. Bull. 25, 122–132 (1977).

    Google Scholar 

  63. Didden, W. A. M. Earthworm communities in grasslands and horticultural soils. Biol. Fert. Soils 33, 111–117 (2001).

    Article  Google Scholar 

  64. Hodge, A., Robinson, D. & Fitter, A. Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci. 5, 304–308 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by a personal VIDI grant from the Netherlands Organization for Scientific Research/Earth and Life Sciences (NWO-ALW) to Jan Willem van Groenigen. We thank Olaf Butenschoen and Bruce A. Snyder for providing standard deviations of their published data for our meta-analysis. We are grateful to Gerlinde De Deyn for giving helpful comments on a previous version of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

IML and JWVG conceived and designed the study, with suggestions and input from SJF and JS; IML extracted the data from the literature and constructed the database; IML and KJVG performed the statistical analysis; IML, JWVG, KJVG, SJF, JS and LB interpreted and discussed the results; IML, JWVG and KJVG wrote the paper, with substantial contributions from all co-authors; JWVG had the overall supervision of the project.

Corresponding author

Correspondence to Ingrid M. Lubbers.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 442 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lubbers, I., van Groenigen, K., Fonte, S. et al. Greenhouse-gas emissions from soils increased by earthworms. Nature Clim Change 3, 187–194 (2013). https://doi.org/10.1038/nclimate1692

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate1692

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing