Skip to main content
Log in

Distribution patterns of the earthworm community in relation to soil properties and metals in agro-ecosystems in Hebei Province, North China

  • Original Article
  • Published:
Community Ecology Aims and scope Submit manuscript

Abstract

In this study, we examined the influence of soil variables (pH, total potassium (TK), available potassium (AK), total nitrogen (TN), total phosphorus (TP), available phosphorus (AP), cation exchange capacity , soil organic carbon (SOC), moisture content (Moisture), subsurface temperature (TEMP), and metal concentrations (Cd, Pb, Cu, and Zn)) on the distribution patterns of earthworm ecological categories, diversity, and species composition in Hebei Province, North China. In total, 535 earthworms were collected from 18 sites, and belonged to three families, six genera, and ten species. Drawida gisti (17.9 inds m−2, 37.8%) and Amynthas hupeiensis (9.3 inds m−2, 39.5%) were the dominant species. The Co-inertia analysis ranking results among the soil factors and earthworms indicated that SOC and AK enhanced the earthworm density (R = 0.76**, p < 0.01; R = 0.77**, p < 0.01). The distribution patterns of epigeic and endogeic species appeared to follow an opposite trend to soil variables (SOC, K, and Moisture) under different agricultural management practices. Anecic species differed considerably from the other ecotypes, and were unaffected by the soil properties (except for TEMP) and metals. The redundancy analysis results showed that the abovementioned dominant species (D. gisti and A. hupeiensis) belong to ecological groups with different propensities for the soil factors (K, P, and SOC). Overall, the soil metal (Cd and Pb) concentrations were not the dominant regressors for the earthworm assemblage. Soil properties (K and SOC) were the main factors affecting earthworm density, category, and species dominance in the study areas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Basker, A., Kirkman, J. H., & Macgregor, A. N. (1994). Changes in potassium availability and other soil properties due to soil ingestion by earthworms. Biology and Fertility of Soils, 17, 154–158.

    Article  CAS  Google Scholar 

  • Bertrand, M., Barot, S., Blouin, M., Whalen, J., de Oliveira, T., & Roger-Estrade, J. (2015). Earthworm services for cropping systems. A review. Agronomy for Sustainable Development, 35(2), 553–567.

    Article  CAS  Google Scholar 

  • Blanchart, E., Albrecht, A., Brown, G. G., Decaëns, T., Duboisset, A., Lavelle, P., Mariani, L., & Roose, E. (2004). Effects of tropical endogeic earthworms on Soil Erosion. Agriculture, Ecosystems & Environment, 104(2), 303–315.

    Article  Google Scholar 

  • Borcard, D., Gillet, F., Legendre, P. 2011. Numerical Ecology with R. 2014–218.

  • Bottinelli, N., Kaupenjohann, M., Mrten, M., Jouquet, P., Soucemarianadin, L., Baudin, F., Tran, T. M., & Rumpel, C. (2020). Age matters: Fate of soil organic matter during ageing of earthworm casts produced by the anecic earthworm Amynthas khami. Soil Biology and Biochemistry, 148, 107906.

    Article  CAS  Google Scholar 

  • Butenschoen, O., Marhan, S., Langel, R., & Scheu, S. (2009). Carbon and nitrogen mobilisation by earthworms of different functional groups as affected by soil sand content. Pedobiologia, 52, 263–272.

    Article  CAS  Google Scholar 

  • Carnovale, D., Baker, G., Bissett, A., & Thrall, P. (2015). Earthworm composition, diversity and biomass under three land use systems in south-eastern Australia. Applied Soil Ecology, 88, 32–40.

    Article  Google Scholar 

  • Chen, Y. (1930). On some new earthworm from Nanking. China Science Report, National Central University, Nanking, 1, 11–37.

  • Chen, Y., Cao, J., He, X., Liu, T., Shao, Y., Zhang, C., Zhou, Q., Li, F., Mao, P., Tao, L., Liu, Z., Lin, Y., Zhou, L., Zhang, W., & Fu, S. (2020). Plant leaf litter plays a more important role than roots in maintaining earthworm communities in subtropical plantations. Soil Biology & Biochemistry, 144, 107777.

    Article  CAS  Google Scholar 

  • Coulis, M., Bernard, L., Gérard, F., Hinsinger, P., Plassard, C., Villeneuve, M., & Blanchart, E. (2014). Endogeic earthworms modify soil phosphorus, plant growth and interactions in a legume-cereal intercrop. Plant and Soil, 379(1–2), 149–160.

    Article  CAS  Google Scholar 

  • Darwin, C., & Murray, J. (1859). On the origin of species by means of natural selection, or, The preservation of favoured races in the struggle for life. London: John Murray, Albemarle Street. https://doi.org/10.5962/bhl.title.82303

    Book  Google Scholar 

  • Datta, S., Singh, J., Singh, S., & Singh, J. (2016). Earthworms, pesticides and sustainable agriculture: A review. Environmental Science and Pollution Research, 23(9), 8227–8243.

    Article  PubMed  Google Scholar 

  • Dray, S., Chessel, D., & Thioulouse, J. (2003). Co-inertia analysis and the linking of ecological tables. Journal of Ecology, 84, 3078–3089.

    Article  Google Scholar 

  • Dulaurent, A., Daoulas, G., Faucon, M., & Houben, D. (2020). Earthworms (Lumbricus terrestris L.) Mediate the Fertilizing Effect of Frass. Agronomy, 10, 783.

    Article  CAS  Google Scholar 

  • Huang, C. D., Ge, Y., Yue, S. Z., Qiao, Y. H., & Liu, L. S. (2021). Impact of soil metals on earthworm communities from the perspectives of earthworm ecotypes and metal bioaccumulation. Journal of Hazardous Materials, 406, 124738.

    Article  PubMed  CAS  Google Scholar 

  • Huang, C. D., Wang, W. Y., Yue, S. Z., Adeel, M., & Qiao, Y. H. (2020). Role of biochar and Eisenia fetida on metal bioavailability and biochar effects on earthworm fitness. Environmental Pollution, 263, 114586.

    Article  PubMed  CAS  Google Scholar 

  • Jamali, M. K., Kazi, T. G., Arain, M. B., Afridi, H. I., Jalbani, N., & Adil, R. S. (2006). The correlation of total and extractable heavy metals from soil and domestic sewage sludge and their transfer to maize (Zea mays L.) plants. Toxicological and Environmental Chemistry, 88, 619–632.

    Article  CAS  Google Scholar 

  • Jun, T., Wei, G., Griffiths, B., Xiaojing, L., Yingjun, X., & Hua, Z. (2012). Maize residue application reduces negative effects of soil salinity on the growth and reproduction of the earthworm Aporrectodea trapezoides, in a soil mesocosm experiment. Soil Biology & Biochemistry, 49, 46–51.

    Article  Google Scholar 

  • Lavelle, P., & Martin, A. (1992). Small-scale and large-scale effects of endogeic earthworms on soil organic matter dynamics in soils of the humid tropics. Soil Biology & Biochemistry, 24(12), 1491–1498.

    Article  Google Scholar 

  • Lévêque, T., Capowiez, Y., Schreck, E., Mazzia, C., Auffan, M., Foucault, Y., Austruy, A., & Dumat, C. (2013). Assessing ecotoxicity and uptake of metals and metalloids in relation to two different earthworm species (Eiseina hortensis and Lumbricus terrestris). Environmental Pollution, 179, 232–241.

    Article  PubMed  Google Scholar 

  • Lévêque, T., Capowiez, Y., Schreck, E., Mombo, S., Mazzia, C., Foucault, Y., & Dumat, C. (2015). Effects of historic metal(loid) pollution on earthworm communities. Science of the Total Environment, 511, 738–746.

    Article  PubMed  Google Scholar 

  • Lowe, C. N., & Butt, K. R. (2007). Earthworm culture, maintenance and species selection in chronic ecotoxicological studies: A critical review. European Journal of Soil Biology, 43, S281–S288.

    Article  CAS  Google Scholar 

  • Mariet, A. L., Gauthier-Manuel, H., Lagiewski, T., Bégeot, C., Walter-Simonnet, A. V., & Gimbert, F. (2020). Impact assessment of legacy wastes from ancient mining activities on current earthworm community. Journal of Hazardous Materials, 393, 122369.

    Article  PubMed  CAS  Google Scholar 

  • Mariotte, P., Le Bayon, R. C., Eisenhauer, N., Guenat, C., & Buttler, A. (2016). Subordinate plant species moderate drought effects on earthworm communities in grasslands. Soil Biology & Biochemistry, 96, 119–127.

    Article  CAS  Google Scholar 

  • Metson, A.J., 1956. Methods of chemical analysis for soil survey samples. N Z Soil Bur Bull No 12.

  • Michaelsen, W. (1928). Miscellanea oligochaetologiea. Arikiv For Zoologl 20(2), 1–60.

  • Michaelsen, W. (1931). The Oligochaeta of China. Peking Natural History Bulletin, 5(2), 1–24.

  • Palm, J., van Schaik, N. L. M. B., & Schröder, B. (2013). Modelling distribution patterns of anecic, epigeic and endogeic earthworms at catchment-scale in agro-ecosystems. Pedobiologia, 56, 23–31.

    Article  Google Scholar 

  • Pascaud, G., Leveque, T., Soubrand, M., Boussen, S., Joussein, E., & Dumat, C. (2014). Environmental and health risk assessment of Pb, Zn, As and Sb in soccer field soils and sediments from mine tailings: Solid speciation and bioaccessibility. Environmental Science and Pollution Research, 21, 4254–4264.

    Article  PubMed  CAS  Google Scholar 

  • Pielou, E. C. (1969). An Introduction to mathematical ecology. New York: Wiley-Interscience.

  • Piotrowska, K., Connolly, J., Finn, J., Black, A., & Bolger, T. (2013). Evenness and plant species identity affect earthworm diversity and community structure in grassland soils. Soil Biology & Biochemistry, 57, 713–719.

    Article  CAS  Google Scholar 

  • R Development Core Team. (2005). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

  • R Core Team. (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

  • Robert, P., & Escoufier, Y. (1976). A unifying tool for linear multivariate statistical methods: The RV-coefficient. Applied Statistics, 25, 257–265.

    Article  Google Scholar 

  • Shahid, M., Xiong, T., Castrec-Rouelle, M., Leveque, T., & Dumat, C. (2013). Water extraction kinetics of metals, arsenic and dissolved organic carbon from industrial contaminated poplar leaves. Journal of Environmental Sciences, 25, 2451–2459.

    Article  CAS  Google Scholar 

  • Shannon, C. E. (1948). A mathematical theory of communication. Bell System Technical Journal, 27, 379–423.

    Article  Google Scholar 

  • Simpson, E. H. (1949). Measurement of diversity. Nature, 163, 688.

    Article  Google Scholar 

  • Singh, S., Sharma, A., Khajuria, K., Singh, J., & Vig, A. P. (2020). Soil properties changes earthworm diversity indices in different agro-ecosystem. BMC Ecology, 20, 1–14.

    Article  CAS  Google Scholar 

  • Sizmur, T., & Richardson, J. (2020). Earthworms accelerate the biogeochemical cycling of potentially toxic elements: Results of a meta-analysis. Soil Biology & Biochemistry, 148, 107865.

    Article  CAS  Google Scholar 

  • Solomou, A. D., Sfougaris, A. I., Vavoulidou, E. M., & Csuzdi, C. (2013). Species richness and density of earthworms in relation to soil factors in olive orchard production systems in Central Greece. Communications in Soil Science and Plant Analysis, 44(1–4), 301–311.

    Article  CAS  Google Scholar 

  • Sun, Y., Li, H., Guo, G., Semple, K. T., & Jones, K. C. (2019). Soil contamination in China: Current priorities, defining background levels and standards for heavy metals. Journal of Environmental Management, 251, 109512.

    Article  PubMed  Google Scholar 

  • Tang, R. G., Ding, C. F., Ma, Y. B., Wang, J. S., Zhang, T. L., & Wang, X. X. (2017). Time-dependent responses of earthworms to soil contaminated with low levels of lead as detected using 1H NMR metabolomics. RSC Advances, 7(54), 34170–34181.

    Article  CAS  Google Scholar 

  • Umiker, K. J., Johnson-Maynard, J. L., Hatten, T. D., Eigenbrode, S. D., & Bosque-Pérez, N. A. (2009). Soil carbon, nitrogen, pH, and earthworm density as influenced by cropping practices in the Inland Pacific Northwest. Soil and Tillage Research, 105, 184–191.

    Article  Google Scholar 

  • Walkley, A. J., & Black, I. A. (1934). Estimation of soil organic carbon by the chromic acid titration method. Soil Science, 37, 29–38.

    Article  CAS  Google Scholar 

  • Wang, K., Qiao, Y. H., Zhang, H. Q., Yue, S. Z., Li, H. F., Ji, X. H., & Crowley, D. (2018). Influence of cadmium-contaminated soil on earthworm communities in a subtropical area of China. Applied Soil Ecology, 127, 64–73.

    Article  Google Scholar 

  • Wang, Z., Gong, X., Zheng, Y., Jin, N., Chen, X., Hu, F., & Liu, M. (2020). Soil protist communities in burrowing and casting hotspots of different earthworm species. Soil Biology and Biochemistry, 144, 107774.

    Article  CAS  Google Scholar 

  • Wu, D., Liu, M. Q., Song, X. C., Jiao, J. G., Li, H. X., & Hu, F. (2015). Earthworm ecosystem service and dis-service in an N-enriched agroecosystem: Increase of plant production leads to no effects on yield-scaled N2O emissions. Soil Biology and Biochemistry, 82, 1–8.

    Article  Google Scholar 

  • Xie, T., Wang, M., Chen, W. P., & Uwizeyimana, H. (2018). Impacts of urbanization and landscape patterns on the earthworm communities in residential areas in Beijing. Science of the Total Environment, 626, 1261–1269.

    Article  PubMed  CAS  Google Scholar 

  • Xu, Q., & Xiao, N. (2010). Terrestrial earthworms (Opisthopora: Oligochaeta) of China. China: China Agricultural Press.

    Google Scholar 

  • Xu, S., Johnson-Maynard, J. L., & Prather, T. S. (2013). Earthworm density and biomass in relation to plant diversity and soil properties in a Palouse prairie remnant. Applied Soil Ecology, 72, 119–127.

    Article  Google Scholar 

  • Yang, W., Ding, J., Wang, S., Yang, Y., Song, G., & Zhang, Y. (2020). Variation in genetic diversity of tree sparrow (Passer montanus) population in long-term environmental heavy metal polluted areas. Environmental Pollution, 263, 11439.

    Article  Google Scholar 

  • Zhang, L., He, N., Chang, D., Liu, X., Zhang, X., Xu, Y., Zhao, C., Sun, J., Li, W., Li, H., Hu, F., & Xu, L. (2018). Does ecotype matter? The influence of ecophysiology on benzo [a]pyrene and cadmium accumulation and distribution in earthworms. Soil Biology & Biochemistry, 121, 24–34.

    Article  CAS  Google Scholar 

  • Zhang, Y. F., & Sun, Z. J. (2014). A new earthworm species of the genus Drawida Michaelsen (Oligochaeta: Moniligastridae) from China. Zoological Systematics, 03(39), 132–134.

    Google Scholar 

  • Zhong, X., Chen, Z., Li, Y., Ding, K., Liu, W., Liu, Y., Yuan, Y., Zhang, M., Baker, A. J. M., Yang, W., Fei, Y., Wang, Y., Chao, Y., & Qiu, R. L. (2020). Factors influencing heavy metal availability and risk assessment of soils at typical metal mines in Eastern China. Journal of Hazardous Materials, 400, 123289.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Natural Science Foundation of Hebei Province (No. C2019204307) and Science and Technology Research Project of Higher Education of Hebei Province (No. ZD2020173), the State Key Laboratory of North China Crop Improvement and Regulation, supported this work.

Funding

Natural Science Foundation of Hebei Province (No. C2019204307); Science and Technology Research Project of Higher Education of Hebei Province (No. ZD2020173).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kun Wang.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 32 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yin, Y., Wang, D., Chen, M. et al. Distribution patterns of the earthworm community in relation to soil properties and metals in agro-ecosystems in Hebei Province, North China. COMMUNITY ECOLOGY 23, 389–399 (2022). https://doi.org/10.1007/s42974-022-00116-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42974-022-00116-4

Keywords

Navigation