Earthworms increase mineral soil nitrogen content – a meta-analysis
Keywords:ecological groups, inorganic nitrogen, mineralization, nitrogen cycle, soil functions
Soil organisms and their interactions play a key role in various ecosystem processes and functions, such as the provision of nutrients. The main actors in nitrogen transformation processes are microorganisms, but earthworms affect these processes as their activity results in changes of the microhabitat and microbial community. Studies have shown that nitrogen content is higher in earthworm casts than in bulk soil, and that earthworm invasion affects soil mineral nitrogen. However, we still lack a quantitative synthesis of earthworm effects on soil nitrogen in bulk soil that integrates the influence of potential controlling factors (i.e., soil properties, climatic conditions and experimental parameters). Here, we investigated the impact of earthworms on soil ammonium (NH4+), nitrate (NO3-) and total mineral nitrogen (ammonium + nitrate, Nmin) using meta-analytic techniques. Earthworms generally increased NO3- (+ 88%) and Nmin (+ 63%), but did not affect NH4+. We assume that earthworms affect total mineral nitrogen mainly by their impact on NO3-. Endogeic and epigeic earthworms significantly increased NO3- and Nmin, whereas no clear effect of anecic earthworms was found. This result is presumably caused by diverse effects of the different ecological groups on the microbial community composition. Our results for mixed ecological groups (i.e., anecic + endogeic earthworms) reveal potentially antagonistic effects of ecological groups. The impact of earthworm presence on NO3- and Nmin increased when experiments lasted longer than one week. The effect of earthworms on NH4+, NO3- or Nmin was not influenced by earthworm abundance and biomass, soil organic carbon, soil C/N ratio, litter C/N ratio, the initial amount of NH4+, NO3- or Nmin, total soil nitrogen or temperature. However, as data availability or replication across factor categories was low for some of these moderators, the non-significant results should be interpreted with caution. Also, we could not investigate interactions among the controlling factors due to paucity of data. Our study thus reveals important knowledge gaps regarding earthworm effects on soil nitrogen. Overall, our results highlight the importance of earthworms for soil nitrogen cycling and strengthen the call for soil-functional models to incorporate soil faunal effects.
Abail, Z. & J. K. Whalen (2019): Nitrous oxide in vivo emission may regulate nitrogen stoichiometry in earthworm body tissues. – European Journal of Soil Biology 91: 25–31.
Adejuyigbe, C. O., G. Tian & G. O. Adeoye (2006): Microcosmic study of soil microarthropod and earthworm interaction in litter decomposition and nutrient turnover. – Nutrient Cycling in Agroecosystems 75: 47–55.
Aira, M., F. Monroy & J. Dominguez (2005): Ageing effects on nitrogen dynamics and enzyme activities in casts of Aporrectodea caliginosa (Lumbricidae). – Pedobiologia 49(5): 467–472.
Amosse, J., P. Turberg, R. Kohler-Milleret, J.-M. Gobat & R.-C. Le Bayon (2015): Effects of endogeic earthworms on the soil organic matter dynamics and the soil structure in urban and alluvial soil materials. – Geoderma 243-244: 50–57.
Anderson, J. M. (1988a): Spatiotemporal effects of invertebrates on soil processes. – Biology and Fertility of Soils 6(3): 216–227.
Anderson, J. M. (1988b): Invertebrate-mediated transport processes in soils. – Agriculture, Ecosystems & Environment 24(1-3): 5–19.
Araujo, Y., F. J. Luizao & E. Barros (2004): Effect of earthworm addition on soil nitrogen availability, microbial biomass and litter decomposition in mesocosms. – Biology and Fertility of Soils 39: 146–152.
Bityutskii, N. P., P. I. Kaidun & K. L. Yakkonen (2012): The earthworm (Aporrectodea caliginosa) primes the release of mobile and available micronutrients in soil. – Pedobiologia 55: 93–99.
Blouin, M., M. E. Hodson, E. A. Delgado, G. Baker, L. Brussaard, K. R. Butt, J. Dai, L. Dendooven, G. Peres, J. E. Tondoh & et al. (2013): A review of earthworm impact on soil function and ecosystem services. – European Journal of Soil Science 64(2): 161–182.
Bohlen, P. J. & C. A. Edwards (1995): Earthworm effects on N dynamics and soil respiration in microcosms receiving organic and inorganic nutrients. – Soil Biology and Biochemistry 27(3): 341–348.
Brown, G.G., P. F. Hendrix & M. H. Beare (1998): Earthworms (Lumbricus rubellus) and the fate of 15N in surface-applied sorghum residues. – Soil Biology & Biochemistry 30(13): 1701–1705.
Brussaard, L. (2012): Ecosystems services provided by the soil biota. – In: Wall, D. H., R. D. Bardgett, V. Behan-Pelletier, J. E. Herrick, T. H. Jones, K. Ritz, J. Six, D. R. Strong & W. H. van der Putten (eds): Soil Ecology and Ecosystems Services – Oxford University Press, Oxford UK: 45–58.
Butt, K. R., J. Frederickson, J. & R. M. Morris (1994): Effect of earthworm density on the growth and reproduction. – Pedobiologia 38(3): 254–261.
Cao, Y., Z. He, T. Zhu & F. Zhao (2021): Organic-C quality as a key driver of microbial nitrogen immobilization in soil: A meta-analysis. – Geoderma 383: 114784.
Caravaca, F. & A. Roldan (2003): Effect of Eisenia foetida earthworms on mineralization kinetics, microbial biomass, enzyme activities, respiration and labile C fractions of three soils treated with a composted organic residue. – Biology and Fertility of Soils 38(1): 45–51.
Creamer, R. E., S. E. Hannula, J. P. V. Leeuwen, D. Stone, M. Rutgers, R. M. Schmelz, P. C. de Ruiter, N. B. Hendriksen, T. Bolger, M. L. Bouffaud et al. (2016): Ecological network analysis reveals the interconnection between soil biodiversity and ecosystem function as affected by land use across Europe. – Applied Soil Ecology 97: 112–124.
Curry, J. & D. Byrne (1992): The role of earthworms in straw decomposition and nitrogen turnover in arable land in Ireland. – Soil Biology and Biochemistry 24(12): 1409–1412.
Devliegher, W. & W. Verstraete (1997): The effect of Lumbricus terrestris on soil in relation to plant growth: Effects of nutrient-enrichment processes (NEP) and gut-associated processes (GAP). – Soil Biology and Biochemistry 29(3/4): 341–346.
Don, A., B. Steinberg, I. Schöning, K. Pritsch, M. Joschko, G. Gleixner & E.-D. Schulze (2008): Organic carbon sequestration in earthworm burrows. – Soil Biology and Biochemistry 40(7): 1803–1812.
Edwards, C. & P. Bohlen (1996): Biology and Ecology of Earthworms. – Chapman and Hall, London: 426 pp.
Farzadfar, S., J. D. Knight & K. A. Congreves (2021): Soil organic nitrogen: an overlooked but potentially significant contribution to crop nutrition. – Plant and Soil 462(1): 7–23.
Ferlian, O., M. P. Thakur, A. Castañeda González, L. M. San Emeterio, S. Marr, B. da Silva Rocha & N. Eisenhauer (2020): Soil chemistry turned upside down: a meta-analysis of invasive earthworm effects on soil chemical properties. – Ecology 101(3): e02936.
Fierer, N., M. S. Strickland, D. Liptzin, M. A. Bradford & C. C. Cleveland (2009): Global patterns in belowground communities. – Ecology Letters 12(11): 1238–1249.
Fraser, P., M. Beare, R. Butler, T. Harrison-Kirk & J. Piercy (2003): Interactions between earthworms (Aporrectodea caliginosa), plants and crop residues for restoring properties of a degraded arable soil. – Pedobiologia 47: 870–876.
Greiner, H. G., D. R. Kashian & S. D. Tiegs (2012): Impacts of invasive Asian (Amynthas hilgendorfi) and European (Lumbricus rubellus) earthworms in a North American temperate deciduous forest. – Biological Invasions 14: 2017–2027.
Groenigen, J. W. v., I. M. Lubbers, H. M. J. Vos, G. G. Brown, D. B. D. Deyn & K. J. v. Groenigen (2014): Earthworms increase plant production: a meta-analysis. – Scientific Reports 4: 6365.
Groenigen, J. W. v., K. J. v. Groenigen, G. F. Koopmans, L. Stokkermans, H. M. J. Vos & I. M. Lubbers (2019): How fertile are earthworm casts? A meta-analysis. – Geoderma 338: 525–535.
Guhra, T., K. Stolze, S. Schweizer & K. U. Totsche (2020): Earthworm mucus contributes to the formation of organo-mineral associations in soil. – Soil Biology and Biochemistry 145: 107785.
Haddaway, N. R., M. J. Page, C. C. Pritchard & L. A. McGuinness (2022): PRISMA2020: An R package and Shiny app for producing PRISMA 2020-compliant flow diagrams, with interactivity for optimised digital transparency and Open Synthesis. – Campbell Systematic Reviews 18: e1230.
Hamamoto, T. & Y. Uchida (2019): The Role of Different Earthworm Species (Metaphire hilgendorfi and Eisenia fetida) on CO2 Emissions and Microbial Biomass during Barley Decomposition. – Sustainability 11: 6544.
Hedges, L. V., J. Gurevitch & P. S. Curtis (1999): The meta-analysis of response ratios in experimental ecology. – Ecology 80(4): 1150–1156.
Helling, B. & O. Larink (1998): Contribution of earthworms to nitrogen turnover in agricultural soils treated with different mineral N-fertilizers. – Applied Soil Ecology 9: 319–325.
Helming, K., K. Daedlow, C. Paul, A.-K. Techen, S. Bartke, B. Bartkowski, D. Kaiser, U. Wollschläger & H.-J. Vogel (2018): Managing soil functions for a sustainable bioeconomy—Assessment framework and state of the art. – Land Degradation & Development 29: 3112–3126.
James, S. W. & T. R. Seastedt (1986): Nitrogen mineralization by native and introduced earthworms - effects on big bluestem growth. – Ecology 67: 1094–1097.
Jana, U., S. Barot, M. Blouin, P. Lavelle, D. Laffray & A. Repellin (2010): Earthworms influence the production of above- and belowground biomass and the expression of genes involved in cell proliferation and stress responses in Arabidopsis thaliana. – Soil Biology & Biochemistry 42: 244–252.
Jun-Zhu, P., Q. Yu-Hui, S. Zhen-Jun, Z. Shuo-Xin, L. Yun-Le & Z. Rui-Qing (2012): Effects of Epigeic Earthworms on Decomposition of Wheat Straw and Nutrient Cycling in Agricultural Soils in a Reclaimed Salinity Area: A Microcosm Study. – Pedosphere 22(5): 726–735.
Kalam, S., A. Basu, I. Ahmad, R. Z. Sayyed, H. A. El–Enshasy, D. J. Dailin & N. L. Suriani (2020): Recent understanding of soil acidobacteria and their ecological significance: A critical review. – Frontiers in Microbiology 11: 2712.
Kielak, A. M., C. C. Barreto, G. A. Kowalchuk, J. A. van Veen & E. E. Kuramae (2016): The ecology of Acidobacteria: Moving beyond genes and genomes. – Frontiers in Microbiology 7: 744.
Kuzyakov, Y. & X. Xu (2013): Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. – New Phytologist 198(3): 656–669.
Lang, B. & D. J. Russell (2022): Excretion of nitrogenous waste by soil fauna and assessment of the contribution to soil nitrogen pools. – Soil Organisms 94(2): 69–83.
Liu, J., L. You, M. Amini, M. Obersteiner, M. Herrero, A. J. B. Zehnder & H. Yang (2010): A high-resolution assessment on global nitrogen flows in cropland. – Proceedings of the National Academy of Sciences 107(17): 8035–8040.
Lubbers, I. M., K. J. van Groenigen, S. J. Fonte, J. Six, L. Brussaard & J. W. van Groenigen (2013): Greenhouse-gas emissions from soils increased by earthworms. – Nature Climate Change 3(3): 187–194.
Makoto, K., Y. Minamiya & N. Kaneko (2016): Differences in soil type drive the intraspecific variation in the responses of an earthworm species and, consequently, tree growth to warming. – Plant and Soil 404: 209–218.
Marhan, S., J. Auber & C. Poll (2015): Additive effects of earthworms, nitrogen-rich litter and elevated soil temperature on N2O emission and nitrate leaching from an arable soil. – Applied Soil Ecology 86: 55–61.
Marhan, S. & S. Scheu (2006): Mixing of different mineral soil layers by endogeic earthworms affects carbon and nitrogen mineralization. – Biology and Fertility of Soils 42(4): 308–314.
McColl, H., P. Hart & F. Cook (1982): Influence of earthworms on some soil chemical and physical properties, and the growth of ryegrass on a soil after topsoil stripping - a pot experiment. – New Zealand Journal of Agricultural Research 25(2): 239–243.
McLean, M. A., S. Migge-Kleian & D. Parkinson (2006): Earthworm invasions of ecosystems devoid of earthworms: effects on soil microbes. – Biological Invasions 8(6): 1257–1273.
Medina-Sauza, R. M., M. Alvarez-Jimenez, A. Delhal, F. Reverchon, M. Blouin, J. A. Guerrero-Analco, C. R. Cerdan, R. Guevara, L. Villain & I. Barois (2019): Earthworms Building Up Soil Microbiota, a Review. – Frontiers in Environmental Science 7: 81.
Neher, D. A. & M. E. Barbercheck (1998): Diversity and function of soil mesofauna. – In: Collins, W. W. & C. O. Qualset (eds): Biodiversity in Agroecosystems. – CRC Press, Boca Raton, FL: 27–47.
Osler, G. H. (2007): Impact of fauna on chemical transformations in soil. – In: Abbott, L. K. & D. V. Murphy (eds): Soil Biological Fertility - A key to Sustainable Land Use in Agriculture. – Springer, The Netherlands: 17–35.
Osler, G. H. R. & M. Sommerkorn (2007): Toward a Complete Soil C and N Cycle: Incorporating the Soil Fauna. – Ecology 88(7): 1611–1621.
Paungfoo-Lonhienne, C., J. Visser, T. G. A. Lonhienne & S. Schmidt (2012): Past, present and future of organic nutrients. – Plant and Soil 359: 1–18.
Phillips, H., C. Guerra, M. Bartz, M. Briones, G. Brown, T. Crowther, O. Ferlian, K. Gongalsky, J. van den Hoogen, J. Krebs et al. (2019): Global distribution of earthworm diversity. – Science 366: 480–485.
Pustejovsky, J. (2020): clubSandwich: Cluster-Robust (Sandwich) Variance Estimators with Small-Sample Corrections. – R package version 0.5.2.
Qiu, J. & M. G. Turner (2017): Effects of non-native Asian earthworm invasion on temperate forest and prairie soils in the Midwestern US. – Biological Invasions 19(1): 73–88.
R Core Team (2021): R: A Language and Environment for Statistical Computing. – R Foundation for Statistical Computing, Vienna, Austria.
Rasband, W. (1997): ImageJ. – U. S. National Institutes of Health, Bethesda, Maryland, USA.
Rurinda, J., S. Zingore, J. M. Jibrin, T. Balemi, K. Masuki, J. A. Andersson, M. F. Pampolino, I. Mohammed, J. Mutegi, A. Y. Kamara & et al. (2020): Science-based decision support for formulating crop fertilizer recommendations in sub-Saharan Africa. – Agricultural Systems 180: 102790.
Ruz-Jerez, B.E., P. R. Ball & R. W. Tillman (1992): 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 Biology and Biochemistry 24(12): 1529–1534.
Salo, T. J., T. Palosuo, K. C. Kersebaum, C. Nendel, C. Angulo, F. Ewert, M. Bindi, P. Calanca, T. Klein, M. Moriondo et al. (2016): Comparing the performance of 11 crop simulation models in predicting yield response to nitrogen fertilization. – Journal of Agricultural Science 154(7): 1218–1240.
Sandor, M. & S. Schrader (2012): Interaction of earthworms and enchytraeids in organically amended soil. – North-Western Journal of Zoology 8(1): 46–56.
Scheu, S. (1987): Microbial activity and nutrient dynamics in earthworm casts (Lumbricidae). – Biology and Fertility of Soils 5(3): 230–234.
Setiyono, T. D., H. Yang, D. T. Walters, A. Dobermann, R. B. Ferguson, D. F. Roberts, D. J. Lyon, D. E. Clay & K. G. Cassman (2011): Maize-N: A Decision Tool for Nitrogen Management in Maize. – Agronomy Journal 103: 1276–1283.
Sheehan, C., L. Kirwan, J. Connolly & T. Bolger (2006): The effects of earthworm functional group diversity on nitrogen dynamics in soils. – Soil Biology & Biochemistry 38(9): 2629–2636.
Sheehan, C., L. Kirwan, J. Connolly & T. Bolger (2007): The effects of earthworm functional group diversity on earthworm community structure. – Pedobiologia 50(6): 479–487.
Shutenko, G. S., B. P. Kelleher, A. J. Simpson, R. Soong, Y. L. Mobarhan & O. Schmidt (2020): Evidence for substantial acetate presence in cutaneous earthworm mucus. – Journal of Soils and Sediments 20: 3627–3632.
Sierra, J., G. Loranger-Merciris, L. Desfontaines & M. Boval (2014): Aerobic microbial activity in four tropical earthworm-soil systems. A mesocosm experiment. – Soil Research 52(6): 584–592.
Singh, J., M. Schädler, W. Demetrio, G. Brown & N. Eisenhauer (2019): Climate change effects on earthworms – a review. – Soil Organisms 91(3): 114–138.
Tanner-Smith, E. E., E. Tipton & J. R. Polanin (2016): Handling complex meta-analytic data structures using robust variance estimates: a tutorial in R. – Journal of Developmental and Life-Course Criminology 2(1): 85–112.
Tiunov, A. V. & S. Scheu (1999): Microbial respiration, biomass, biovolume and nutrient status in burrow walls of Lumbricus terrestris L. (Lumbricidae). – Soil Biology and Biochemistry 31(14): 2039–2048.
Tiunov, A. V. & S. Scheu (2000): Microbial biomass, biovolume and respiration in Lumbricus terrestris L. cast material of different age. – Soil Biology & Biochemistry 32(2): 265–275.
Turbé, A., A. D. Toni, P. Benito, P. Lavelle, P. Lavelle, N. R. Camacho, W. H. van der Putten, E. Labouze & S. Mudgal (2010): Soil biodiversity: functions, threats and tools for policy makers. – Bio Intelligence Service, IRD, and NIOO, Report for European Commission (DG Environment): 250 pp.
USDA Natural Resources Conservation Service, Soil Survey Staff (2019): Soil Texture Calculator. Natural Resources Conservation Service, United States Department of Agriculture [https://www.nrcs.usda.gov/wps/portal/nrcs/detailfull/soils/research/guide/?cid=NRCS142P2_054167, Accessed 2021-05-11]
Uvarov, A. V. (2009): Inter- and intraspecific interactions in lumbricid earthworms: Their role for earthworm performance and ecosystem functioning. – Pedobiologia 53(1): 1–27.
Viechtbauer, W. (2010): Conducting meta-analyses in R with the metafor package. – Journal of Statistical Software 36(3): 1–48.
Vogel, H.-J., S. Bartke, K. Daedlow, K. Helming, I. Kögel-Knabner, B. Lang, E. Rabot, D. Russell, B. Stößel, U. Weller & et al. (2018): A systemic approach for modeling soil functions. – SOIL 4: 83–92.
Whalen, J. K., R. W. Parmelee & S. Subler (2000): Quantification of nitrogen excretion rates for three Lumbricid earthworms using 15N. – Biology and Fertility of Soils 32(4): 347–352.
Willems, J., J. Marinissen & J. Blair (1996): Effects of earthworms on nitrogen mineralization. – Biology and Fertility of Soils 23(1): 57–63.
Wu, Y., J. Liu, M. Shaaban & R. Hu (2021): Dynamics of soil N2O emissions and functional gene abundance in response to biochar application in the presence of earthworms. – Environmental Pollution 268: 115670.
Wu, Y., M. Shaaban, J. Zhao, R. Hao & R. Hu (2015): Effect of the earthworm gut-stimulated denitrifiers on soil nitrous oxide emissions. – European Journal of Soil Biology 70: 104–110.
Xue, R., C. Wang, X. Liu & M. Liu (2022): Earthworm regulation of nitrogen pools and dynamics and marker genes of nitrogen cycling: A meta-analysis. – Pedosphere 32(1): 131–139.
Zheng, Y., S. Wang, M. Bonkowski, X. Chen, B. Griffiths, F. Hu & M. Liu (2018): Litter chemistry influences earthworm effects on soil carbon loss and microbial carbon acquisition. – Soil Biology & Biochemistry 123: 105–114.
How to Cite
LicenseCopyright (c) 2023 SOIL ORGANISMS
All articles from Senckenberg’s SOIL ORGANISMS Open Access scientific journal that are made available on the Senckenberg website (www.senckenberg.de) and also www.soil-organisms.org may be read, copied, distributed, and (in limited quantity) printed for non-commercial, private, scientific purposes.
In accordance with the German Science Foundation’s „Rules for the Safeguarding of Good Scientific Practice“, references to cited articles are to be complete and correct and furnished with a link to the website of the Senckenberg journal in question.
The Senckenberg Society for Nature Research (Senckenberg Gesellschaft für Naturforschung, SGN) is a member of the Leibniz Association (Leibniz-Gemeinschaft) and is therefore committed to the idea of Open Access as explained in the Berlin Declaration (Berlin Declaration on Open Access to Scientific Knowledge, Berliner Erklärung über den offenen Zugang zu wissenschaftlichem Wissen).
Open Access is understood to mean the charge-exempt public access to scientific results via the internet. The users should be able to read, copy, print, search within, and reference the full text without limitation and to use it in any conceivable lawful manner without financial, legal or technical hindrance.
This applies also to the SGN, which publishes various scientific series. Some scientific journals are made available to the public via Open Acess in addition to printed copies.