Balancing sampling effort and representativeness for assessing species composition of Enchytraeidae in different habitats

Authors

DOI:

https://doi.org/10.25674/514

Keywords:

soil fauna, rarefaction, singletons, seasonal variation, edaphobase data warehouse

Abstract

Soil biodiversity has gained increased attention in science as well as policy during the last years, and programs for monitoring soil animal biodiversity have been approved. Enchytraeidae are often part of these programs, however, their identification to species level is time consuming and experts are rare. Probably, reducing the number of samples taken can increase efficiency of investigating enchytraeid communities, thereby reducing effort not only for morphological identification by taxon experts but also possibly for molecular approaches. However, the trade-off between effort and quality of the received data needs to be addressed carefully. To test the potential for reduction in sample number without losing important information, we used an existing high-effort dataset of enchytraeid communities from German grasslands, forests, and arable fields. We applied species rarefaction and estimates of expected biodiversity given the existing dataset to find out if the number of soil cores taken, or the number of sampling events, can safely be reduced without losing important information on indicator species. Our results show that, while missing out only very sporadic species, sampling effort can be reduced from the initial 20 soil cores by 55 % in coniferous forests, 45 % in broadleaved forests, 40 % in grasslands, and 30 % in arable fields. Despite the fact that species accumulation curves were not significantly affected, a reduction of sampling frequency from two (spring and fall) to only one (either spring or fall) resulted in the consistent reduction of the number of indicator species across different habitats. If sampling effort needs to be restricted, we therefore recommend a reduction in total number of soil cores rather than a reduction of sampling times.

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References

Anthony, M. A., Bender, S. F., & van der Heijden, M. G. A. (2023). Enumerating soil biodiversity. Proceedings of the National Academy of Sciences, 120. https://doi.org/10.1073/pnas

Ballasus, H., Lachmann, C., Weiß, L., Nabel, M., Lenzen, J., Pieper, S., Glante, F., Höper, H., Fröhlich, J., Walter, , et al. (2026). Konzept für ein bundesweites Biodiversitätsmonitoring – Grundlagen und bundesweite Ersterfassung. https://doi.org/10.5281/zenodo.20152935

Bardgett, R. D. (2005). The biology of soil: A community and ecosystem approach (1st ed.). Oxford University Press.

Beylich, A., & Graefe, U. (2002). Annelid coenoses of wetlands representing different decomposer communities. In G. Broll, W. Merbach, & E.-M. Pfeiffer (Eds.), Wetlands in Central Europe (pp. 1–10). Springer.

Bonkowski, M., & Roy, J. (2012). Decomposer community complexity affects plant competition in a model early successional grassland community. Soil Biology and Biochemistry, 46, 41–48. https://doi.org/10.1016/j.soilbio.2011.11.013

Briones, M. J. I., Poskitt, J., & Ostle, N. (2004). Influence of warming and enchytraeid activities on soil CO2 and CH4 fluxes. Soil Biology and Biochemistry, 36, 1851–1859. https://doi.org/10.1016/j.soilbio.2004.04.039

Conti, E., & Mulder, C. (2022). Chemistry-driven Enchytraeidae assemblages acting as soil and ecosystem engineers in edaphic communities. Ecological Indicators, 144, 109529. https://doi.org/10.1016/j.ecolind.2022.109529

Creamer, R. E., Hannula, S. E., Leeuwen, J. P. V., Stone, D., Rutgers, M., Schmelz, R. M., Ruiter, P. C., Hendriksen, N. B., Bolger, T., Bouffaud, M.-L., et al. (2016). Ecological network analysis reveals the inter-connection between soil biodiversity and ecosystem function as affected by land use across Europe. Applied Soil Ecology, 97, 112–124. https://doi.org/10.1016/j.apsoil.2015.08.006

Cuartero, J., Briones, M. J. I., Rast, B. M., Stierli, B., Maurer-Troxler, C., Hug, A. S., Widmer, F., Schlaghamerský, J., & Frey, B. (2025). Earthworm and enchytraeid indicator taxa of different land-use types identified using soil DNA metabarcoding. Applied Soil Ecology, 206, 105891. https://doi.org/10.1016/j.apsoil.2025.105891

De Cáceres, M., Legendre, P., Wiser, S. K., & Brotons, L. (2012). Using species combinations in indicator value analyses. Methods in Ecology and Evolution, 3, 973–982. https://doi.org/10.1111/j.2041-210X.2012.00246.x

Degtyarev, M. I., Korobushkin, D. I., Gongalsky, K. B., & Zaitsev, A. S. (2019). Enchytraeid community (Annelida, Clitellata, Enchytraeidae) and its dependence on edaphic conditions in rice agroecosystems in Russia. Russian Journal of Ecology, 50, 384–390.

Dósza-Farkas, K. (1973). Saisondynamische Untersuchungen des Enchytraeiden-Besatzes im Boden eines ungarischen Quercetum petraeae cerris. Pedobiologia, 13, 361–367.

European Parliament and the Council of the European Union. (2025). Directive (EU) 2025/2360 of the European Parliament and of the Council of 12 November 2025 on soil monitoring and resilience (Soil Monitoring Law). https://eur-lex.europa.eu/eli/dir/2025/2360/oj

Filser, J., Faber, J. H., Tiunov, A. V., Brussaard, L., Frouz, J., De Deyn, G., Uvarov, A. V., Berg, M. P., Lavelle, P., Loreau, M., et al. (2016). Soil fauna: Key to new carbon models. SOIL, 2, 565–582. https://doi.org/10.5194/soil-2-565-2016

Gao, C., & Dusa, A. (2026). ggVennDiagram: A ‘ggplot2’ implement of Venn diagram (Version 1.5.7) [R package]. https://doi.org/10.32614/CRAN.package.ggVennDiagram

Gotelli, N. J., & Colwell, R. K. (2001). Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters, 4, 379–391. https://doi.org/10.1046/j.1461-0248.2001.00230.x

Graefe, U., & Schmelz, R. M. (1999). Indicator values, strategy types and life forms of terrestrial Enchytraeidae and other microannelids. Newsletter on Enchytraeidae, 6, 59–67.

Ingimarsdóttir, M., Caruso, T., Ripa, J., Magnúsdóttir, Ó. B., Migliorini, M., & Hedlund, K. (2012). Primary assembly of soil communities: Disentangling the effect of dispersal and local environment. Oecologia, 170, 745–754. https://doi.org/10.1007/s00442-012-2334-8

John, K., Zaitsev, A. S., & Wolters, V. (2021). Soil fauna groups respond differentially to changes in crop rotation cycles in rice production systems. Pedobiologia, 84, 150703. https://doi.org/10.1016/j.pedobi.2020.150703

Jänsch, S., Römbke, J., & Didden, W. (2005). The use of enchytraeids in ecological soil classification and assessment concepts. Ecotoxicology and Environmental Safety, 62, 266–277. https://doi.org/10.1016/j.ecoenv.2004.10.025

Józefowska, A., Wos, B., Pietrzykowski, M., & Schlaghamerský, J. (2020). Colonisation by enchytraeids as a suitable indicator of successful biological reclamation of post-mining technosols using alders. Applied Soil Ecology, 145. https://doi.org/10.1016/j.apsoil.2019.06.003

Korobushkin, D. I., Guseva, P. A., Gongalsky, K. B., Saifutdinov, R. A., Zaitsev, A. S., & Degtyarev, M. I. (2024). Are there different trophic niches of enchytraeids? A stable isotopic (δ13C, δ15N) evidence. Soil Biology and Biochemistry, 194, 109422. https://doi.org/10.1016/j.soilbio.2024.109422

Lehmitz, R., Russell, D. J., Hohberg, K., Christian, A., & Xylander, W. E. R. (2012). Active dispersal of oribatid mites into young soils. Applied Soil Ecology, 55, 10–19.

Liiri, M., Ilmarinen, K., & Setälä, H. (2002). The significance of Cognettia sphagnetorum (Enchytraeidae) on nitrogen availability and plant growth in wood ash-treated humus soil. Plant and Soil, 246, 31–39. https://doi.org/10.1023/A:1021515313890

Lundkvist, H. (1981). Enchytraeidae (Oligochaeta) in pine forest soils: Population dynamics and response to environmental changes. Doctoral thesis. Uppsala University.

Martinsson, S., & Erséus, C. (2014). Cryptic diversity in the well-studied terrestrial worm Cognettia sphagnetorum (Clitellata: Enchytraeidae). Pedobiologia, 57(1), 27–35.

Martinsson, S., Rota, E., & Erséus, C. (2015). Revision of Cognettia (Clitellata, Enchytraeidae): Reestablishment of Chamaedrilus and description of cryptic species in the sphagnetorum complex. Systematics and Biodiversity, 13, 257–277.

Ojala, R., & Huhta, V. (2001). Dispersal of microarthropods in forest soil. Pedobiologia, 45, 443–450.

Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P. M., et al. (2020). vegan: Community Ecology Package. https://cran.r-project.org/package=vegan

Oliverio, A. M., Gan, H., Wickings, K., & Fierer, N. (2018). A DNA metabarcoding approach to characterize soil arthropod communities. Soil Biology and Biochemistry, 125, 37–43. https://doi.org/10.1016/j.soilbio.2018.06.026

O’Connor, F. B. (1967). The Enchytraeidae. In A. Burges & R. Raw (Eds.), Soil biology (pp. 213–257). Academic Press.

Pelosi, C., & Römbke, J. (2016). Are Enchytraeidae (Oligochaeta, Annelida) good indicators of agricultural management practices? Soil Biology and Biochemistry, 100, 255–263. https://doi.org/10.1016/j.soilbio.2016.06.030

Petersen, H., & Luxton, M. (1982). A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos, 39, 288–388.

Postma-Blaauw, M. B., De Goede, R. G. M., Bloem, J., Faber, J. H., & Brussaard, L. (2010). Soil biota community structure and abundance under agricultural intensification and extensification. Ecology, 91, 460–473.

R Foundation for Statistical Computing. (2025). R version 4.5.1 (2025-06-13 ucrt): Great Square Root [Computer software].

Remelli, S., Gruss, I., & Menta, C. (2026). Advances in soil arthropod identification: Integrating morphological, molecular, and AI-based approaches. European Journal of Soil Biology, 128, 103812. https://doi.org/10.1016/j.ejsobi.2026.103812

Römbke, J., Jänsch, S., Höfer, H., Horak, F., Roß-Nickoll, M., Russell, D. J., & Toschki, A. (2013). State of knowledge of enchytraeid communities on German soils as a basis for biological soil quality assessment. Soil Organisms, 85, 123–146.

Saito, V. S., Fonseca-Gessner, A. A., & Siqueira, T. (2015). How should ecologists define sampling effort? The potential of Procrustes analysis for studying variation in community composition. Biotropica, 47, 399–402. https://doi.org/10.1111/btp.12222

Schlaghamerský, J. (2002). The Enchytraeidae of spruce forest plots of different exposure and acid deposition in a German mountain range. European Journal of Soil Biology, 38, 305–309. https://doi.org/10.1016/S1164-5563(02)01164-0

Schlaghamerský, J. (2010). The small annelids (Annelida: Enchytraeidae, Rhyacodrilinae, Aeolosomatidae) in soils of three forests in the White Carpathians (Czech Republic). Acta Societatis Zoologicae Bohemicae, 74, 103–115.

Schlaghamerský, J., & Kobetičová, K. (2005). A small annelid community (Enchytraeidae, Tubificidae, Aeolosomatidae) during meadow restoration on arable land and in a nearby well-preserved meadow. Proceedings of the Estonian Academy of Sciences: Biology and Ecology, 54, 323–330.

Schmelz, R. M. (2016a). Edaphobase Länderstudien Bayern Enchytraeidae [Data set]. Edaphobase. https://portal.edaphobase.org/

Schmelz, R. M. (2016b). Edaphobase Länderstudien NP Eifel Enchytraeidae [Data set]. Edaphobase. https://portal.edaphobase.org/

Schmelz, R. M. (2016c). Edaphobase Länderstudien Sachsen Enchytraeidae [Data set]. Edaphobase. https://portal.edaphobase.org/

Schmelz, R. M. (2016d). Edaphobase Länderstudien Sachsen-Anhalt Enchytraeidae [Data set]. Edaphobase. https://portal.edaphobase.org/

Schmelz, R. M., & Collado, R. (2010). A guide to European terrestrial and freshwater species of Enchytraeidae. Soil Organisms, 82, 1–176. https://doi.org/10.1007/978-94-017-5279-4_3

Serbource, C., Sammartino, S., Cornu, S., Papillon, J., Adrien, J., & Pelosi, C. (2025). Enchytraeids: Small but important ecosystem engineers. Geoderma, 453, 4–10.

Sgarbi, L. F., Bini, L. M., Heino, J., Jyrkänkallio-Mikkola, J., Landeiro, V. L., Santos, E. P., Schneck, F., Siqueira, T., Soininen, J., Tolonen, K. T., & Melo, A. S. (2020). Sampling effort and information quality provided by rare and common species in estimating assemblage structure. Ecological Indicators, 110. https://doi.org/10.1016/j.ecolind.2019.105937

Toschki, A., Burkhardt, U., Haase, H., Höfer, H., Jänsch, S., Oellers, J., Römbke, J., Roß-Nickoll, M., Salamon, J.-A., Schmelz, R. M., Scholz-Starke, B., & Russell, D. J. (2021). Die Edaphobase-Länderstudien: Synökologische Untersuchungen von Bodenorganismen in einem Biotop- und Standortgradienten in Deutschland 2014–2018. Peckiana, 14, 1–367.

Van Vliet, P. C. J., Coleman, D. C., & Hendrix, P. F. (1997). Population dynamics of Enchytraeidae (Oligochaeta) in different agricultural systems. Biology and Fertility of Soils, 25, 123–129. https://doi.org/10.1007/s003740050291

Vandewalle, M., de Bello, F., Berg, M. P., Bolger, T., Dolédec, S., Dubs, F., Feld, C. K., Harrington, R., Harrison, P. A., Lavorel, S., et al. (2010). Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodiversity and Conservation, 19, 2921–2947. https://doi.org/10.1007/s10531-010-9798-9

Ventins, J., & Melecis, V. (2025). Boreal forest enchytraeids (Clitellata, Enchytraeidae) population increase due to precipitation: Long-term data from Latvia. Applied Soil Ecology, 206, 105882. https://doi.org/10.1016/j.apsoil.2025.105882

Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer.

Yeates, G. W., Wardle, D. A., & Watson, R. N. (1999). Responses of soil nematode populations, community structure, diversity and temporal variability to agricultural intensification over a seven-year period. Soil Biology and Biochemistry, 31, 1721–1733.

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Published

2026-11-10

How to Cite

Scheunemann, N., Beylich, A., & Schmelz, R. M. (2026). Balancing sampling effort and representativeness for assessing species composition of Enchytraeidae in different habitats. Soil Organisms, 98(Special Issue 2), 65–78. https://doi.org/10.25674/514

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