Soil mineral nitrogen content is increased by soil mesofauna and nematodes – a meta-analysis
DOI:
https://doi.org/10.25674/so95iss2id310Keywords:
Inorganic nitrogen, microfauna, mineralization, nitrogen cycle, soil faunaAbstract
The world’s soils maintain various ecosystem processes and functions, such as the provision of nitrogen, which is the basis for plant growth. Microorganisms are the key actors in nitrogen transformation processes, but soil fauna can also affect nitrogen cycling , e.g. through food-web interactions or by changing the soil habitat. Several individual studies report increases of soil nitrogen due to soil meso- or microfaunal effects. Recent meta-analyses have shown that nitrogen content and fertility of soils is substantially increased by earthworms. However, we still lack a quantitative synthesis of the influence of smaller soil fauna on soil nitrogen. We present a meta-analysis of effects of soil mesofauna (i.e. enchytraeidae, springtails, mites) and microfauna (i.e. nematodes) on ammonium (NH4+), nitrate (NO3-), and total mineral nitrogen (ammonium + nitrate, Nmin). We furthermore investigated whether the faunal effects depend on functional characteristics (i.e. trophic groups or size classes) or faunal density; or were modulated by experimental conditions or soil characteristics. Our results show that soil meso- and microfauna generally increased NO3- and Nmin concentrations, but did not affect NH4+. Increases of soil nitrogen are found in presence of microbi-detritivores or faunal communities that span various trophic levels. Micro- and mesofauna improve nitrogen availability in the soil in short- to intermediate term of up to two months. Furthermore, the provision of organic material plays an important role, as micro- and mesofauna have a positive effect on soil nitrogen especially when organic material is added and incorporated into the soil. This has important implications for agricultural management with regards to handling of organic residues. No significant moderating influence of micro- and mesofaunal density, litter C:N ratio, soil organic-carbon content, initial amount of NH4+, NO3- or Nmin, or experimental temperature was found. However, data availability or replication across factor categories was low for some of these moderators, and we could not differentiate between size classes (i.e., micro- or mesofauna) for all moderators or investigate interactions among different moderators. Thus, our study reveals important knowledge gaps that should be addressed in future research. Overall, our results underline the role of micro- and mesofauna for soil nitrogen cycling.
References
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(1-3): 47–55.
Anderson, R., W. Gould, L. Woods, C. Cambardella, R. Ingham & D. Coleman (1983): Organic and inorganic nitrogenous losses by microbivorous nematodes in soil. – Oikos 40(1): 75–80.
Beare, M. H., R. W. Parmelee, P. F. Hendrix, W. Cheng, D. C. Coleman, & D. A. Crossley (1992): Microbial and faunal interactions and effects on litter nitrogen and decomposition in agroecosystems. – Ecological Monographs 62(4): 569–591.
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.
Bouwman, L., J. Bloem, P. Vandenboogert, F. Bremer, G. Hoenderboom & P. C. DeRuiter (1994): Short-term and long-term effects of bacterivorous nematodes and nematophagous fungi on carbon and nitrogen mineralization in microcosms. – Biology and Fertility of Soils 17(4): 249–256.
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.
Brussaard, L., R. Noordhuis, M. Geurs & L. Bouwman (1995): Nitrogen mineralization in soil in microcosms with or without bacterivorous nematodes and nematophagous mites. – Acta Zoologica Fennica 196: 15–21.
Crowther, T. W., L. Boddy & T. H. Jones (2012): Functional and ecological consequences of saprotrophic fungus-grazer interactions. – ISME Journal 6(11): 1992–2001.
Djigal, D., M. Sy, A. Brauman, T. A. Diop, D. Mountport, J. L. Chotte & C. Villenave (2004): Interactions between Zeldia Punctata (Cephalobidae) and bacteria in the presence or absence of maize plants. – Plant and Soil 262(1-2): 33–44.
Eisenhauer, N., A. Vogel, B. Jensen & S. Scheu (2018): Decomposer diversity increases biomass production and shifts aboveground-belowground biomass allocation of common wheat. – Scientific Reports 8: 17894.
Engell, I., D. Linsler, S. Schrader, A. Taylor, B. Ludwig & M. Potthoff (2021): Crop residue displacement by soil inversion: Annelid responses and their impact on carbon and nitrogen dynamics in a lab-based mesocosm study. – Applied Soil Ecology 167: 104151.
Ferris, H. & M. Matute (2003): Structural and functional succession in the nematode fauna of a soil food web. – Applied Soil Ecology 23(2): 93–110.
Gebremikael, M. T., D. Buchan & S. De Neve (2014): Quantifying the influences of free-living nematodes on soil nitrogen and microbial biomass dynamics in bare and planted microcosms. – Soil Biology & Biochemistry 70: 131–141.
Gebremikael, M. T., H. Steel, D. Buchan, W. Bert & S. De Neve (2016): Nematodes enhance plant growth and nutrient uptake under C and N-rich conditions. – Scientific Reports 6: 32862.
de Graaff, M.-A., J. Adkins, P. Kardol & H. L. Throop (2015): A meta-analysis of soil biodiversity impacts on the carbon cycle. – Soil 1(1): 257–271.
Griffiths, B. S. (1986): Mineralization of nitrogen and phosphorus by mixed cultures of the ciliate protozoan Colpoda steinii, the nematode Rhabditis sp. and the bacterium Pseudomonas fluorescens. – Soil Biology & Biochemistry 18(6): 637–641.
Griffiths, B. S. (1989): Enhanced nitrification in the presence of bacteriophagous protozoa. – Soil Biology and Biochemistry 21: 1045–1051.
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.
Haimi, J. & A. Siira-Pietkainen (2003): Activity and role of the enchytraeid worm Cognettia sphagnetorum (Vejd.) (Oligochaeta: Enchytraeidae) in organic and mineral forest soil. – Pedobiologia 47(4), 303–310.
Hassink, J., L. A. Bouwman, K. B. Zwart & L. Brussaard (1993a): Relationships between habitable pore space, soil biota and mineralization rates in grassland soils. – Soil Biology and Biochemistry 25(1):1150–1156.
Hassink, J., L. A. Bouwman, K. B. Zwart, J. Bloem & L. Brussaard (1993b): Relationships between soil texture, physical protection of organic matter, soil biota, and C and N mineralization in grassland soils. – Geoderma 57(1-2): 105–128.
Hedges, L. V., J. Gurevitch & P. S. Curtis (1999): The meta-analysis of response ratios in experimental ecology. – Ecology 80(4): 1150–1156.
Holajjer, P., A. Kamra & P. Singh (2016): Influence of nematode-bacterial interactions on N and P mineralisation in soil and on decomposition of crop residues during aerobic composting. – Applied Ecology and Environmental Research 14(2): 283–299.
Holland, E. A. & D. C. Coleman (1987): Litter placement effects on microbial and organic matter dynamics in an agroecosystem. – Ecology 68(2): 425–433.
Ingham, R. E., J. Trofymow, E. R. Ingham & D. C. Coleman (1985): Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. – Ecological Monographs 55(1): 119–140.
Kaneda, S. & N. Kaneko (2008): Collembolans feeding on soil affect carbon and nitrogen mineralization by their influence on microbial and nematode activities. – Biology and Fertility of Soils 44: 435–442.
Kaneda, S. & N. Kaneko (2011): Influence of Collembola on nitrogen mineralization varies with soil moisture content. – Soil Science and Plant Nutrition 57(1): 40–49.
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.
Lang, B., B. Betancur-Corredor & D. J. Russell (2023): Earthworms increase mineral soil nitrogen content–a meta-analysis. Soil Organisms 95(1): 1–16.
Maraun, M., H. Martens, S. Migge, A. Theenhaus & S. Scheu (2003): Adding to `the enigma of soil animal diversity’: fungal feeders and saprophagous soil invertebrates prefer similar food substrates. – European Journal of Soil Biology 39: 85–95.
Mamilov, A., B. Byzov, D. Zvyagintsev & O. Dilly (2001): Predation on fungal and bacterial biomass in a soddy-podzolic soil amended with starch, wheat straw and alfalfa meal. – Applied Soil Ecology 16(2): 131–139.
Mebes, K.-H. & J. Filser (1998): Does the species composition of Collembola affect nitrogen turnover? – Applied Soil Ecology 9(1): 241 – 247.
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.
Moher, D., A. Liberati, J. Tetzlaff, D. G. Altman & The PRISMA Group (2009): Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. – PloS Medicine 6 (7): e1000097.
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. R. & M. Sommerkorn (2007): Toward a Complete Soil C and N Cycle: Incorporating the Soil Fauna. – Ecology 88(7): 1611–1621.
Pelosi, C. & J. Roembke (2018): Enchytraeids as bioindicators of land use and management. – Applied Soil Ecology 123(SI): 775–779.
Porre, R. J., J. W. v. Groenigen, G. B. De Deyn, R. G. M. de Goede & I. M. Lubbers (2016): Exploring the relationship between soil mesofauna, soil structure and N2O emissions. – Soil Biology & Biochemistry 96: 55–64.
Postma-Blaauw, M. B., F. T. de Vries, R. G. M. de Goede, J. Bloem, J. H. Faber & L. Brussaard (2005): Within-trophic group interactions of bacterivorous nematode species and their effects on the bacterial community and nitrogen mineralization. – Oecologia 142(3): 428–439.
Pustejovsky, J. (2020): clubSandwich: Cluster-Robust (Sandwich) Variance Estimators with Small-Sample Corrections. – R package version 0.5.2.
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.
Ronn, R. M., B. S. Griffiths & I. M. Young (2001): Protozoa, nematodes and N-mineralization across a prescribed soil textural gradient. – Pedobiologia 45(6): 481–495.
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.
Schneider, K., C. Renker & M. Maraun (2005): Oribatid mite (Acari, Oribatida) feeding on ectomycorrhizal fungi. – Mycorrhiza 16: 67–72.
Sulkava, P., V. Huhta & J. Laakso (1996): Impact of soil faunal structure on decomposition and N-mineralisation in relation to temperature and moisture in forest soil. – Pedobiologia 40(6): 505–513.
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.
Thakur, M. P. & S. Geisen (2019): Trophic regulations of the soil microbiome. – Trends in Microbiology 27(9): 771–780.
Thakur, M. P., J. W. v. Groenigen, I. Kuiper & G. B. De Deyn (2014): Interactions between microbial-feeding and predatory soil fauna trigger N2O emissions. – Soil Biology & Biochemistry 70: 256–262.
Trap, J., M. Bonkowski, C. Plassard, C. Villenave & E. Blanchart (2016): Ecological importance of soil bacterivores for ecosystem functions. – Plant and Soil 398: 1–24.
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 2022-01-12].
Vedder, B., C. Kampichler, G. Bachmann, A. Bruckner & E. Kandeler (1996): Impact of faunal complexity on microbial biomass and N turnover in field mesocosms from a spruce forest soil. – Biology and Fertility of Soils 22(1-2): 22–30.
Verhoef, H. A. & L. Brussaard (1990): Decomposition and nitrogen mineralization in natural and agroecosystems: the contribution of soil animals. – Biogeochemistry 11(3): 175–211.
Viechtbauer, W. (2010): Conducting meta-analyses in R with the metafor package. – Journal of Statistical Software 36(3): 1–48.
van Vliet, P. C. J., M. H. Beare, D. C. Coleman & P. E. Hendrix (2004): Effects of enchytraeids (Annelida: Oligochaeta) on soil carbon and nitrogen dynamics in laboratory incubations. – Applied Soil Ecology 25(2): 147–160.
Woods, L. E., C. V. Cole, E. T. Elliott, R. V. Anderson & D. C. Coleman (1982): Nitrogen transformations in soil as affected by bacterial-microfaunal interactions. – Soil Biology and Biochemistry 14(2): 93–98.
Xiao, H., B. Griffiths, X. Chen, M. Liu, J. Jiao, F. Hu & H. Li (2010): Influence of bacterial-feeding nematodes on nitrification and the ammonia-oxidizing bacteria (AOB) community composition. – Applied Soil Ecology 45(3): 131–137.
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.
Zhu, T., C. Yang, J. Wang, S. Zeng, M. Liu, J. Yang, B. Bai, J. Cao, X. Chen & C. Müller (2018): Bacterivore nematodes stimulate soil gross N transformation rates depending on their species. – Biology and Fertility of Soils 54: 107–118.
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