Abstract
The conversion of natural habitats into farmland has been a leading cause of species loss worldwide. Here, we investigated to what extent less intensive soil disturbance can mitigate this loss. Specifically, we examined whether reduced soil disturbance by tillage in agricultural fields could contribute to soil microbial biodiversity by providing a habitat for species that are limited by conventional tillage. To do so, we studied the diversity of soil biotas from three agricultural practices representing conventional tillage, reduced tillage and no tillage. Study fields were sampled by taking a bulk soil sample at the centre and edge of each field. The soil communities were recorded with environmental DNA metabarcoding using three molecular markers targeting bacteria, fungi and eukaryotes. While these three markers represent the vast majority of biotic variation in the soil, they will inevitably be dominated by the megadiverse microbiota of bacteria, microfungi and protists. We found a significant differentiation in community composition related to the intensity of tillage. Richness was weakly correlated to tillage, and more influenced by whether the sample was taken in the center or the edge of the field. Despite the significant effect of tillage on composition, comparisons with natural ecosystems revealed that all 30 study fields were much more similar in composition to other rotational fields than to more natural habitats, oldfields and leys. Despite a slightly higher similarity to oldfields and semi-natural grasslands, the contribution of no-till soil communities to biodiversity conservation is negligible, and our results indicate that restoration on set aside land may contribute more to conservation.
Similar content being viewed by others
References
Bálint, M., M. Bahram, A.M. Eren, K. Faust, J.A. Fuhrman, B. Lindahl, R.B. O’Hara, M. Öpik, et al. 2016. Millions of reads, thousands of taxa: Microbial community structure and associations analyzed via marker genes. FEMS Microbiology Reviews 40: 686–700.
Bender, S.F., C. Wagg, and M.G. van der Heijden. 2016. An underground revolution: Biodiversity and soil ecological engineering for agricultural sustainability. Trends in Ecology & Evolution 31: 440–452.
Bengtsson, J., J. Ahnström, and A.C. Weibull. 2005. The effects of organic agriculture on biodiversity and abundance: A meta-analysis. Journal of Applied Ecology 42: 261–269.
Brennan, A., T. Fortune, and T. Bolger. 2006. Collembola abundances and assemblage structures in conventionally tilled and conservation tillage arable systems. Pedobiologia 50: 135–145.
Briones, M.J.I., and O. Schmidt. 2017. Conventional tillage decreases the abundance and biomass of earthworms and alters their community structure in a global meta-analysis. Global Change Biology 23: 4396–4419.
Brunbjerg, A.K., H.H. Bruun, K. Brøndum, A.T. Classen, L. Dalby, K. Fog, T.G. Frøslev, I. Goldberg, et al. 2019. A systematic survey of regional multi-taxon biodiversity: Evaluating strategies and coverage. BMC Ecology 19: 1–15.
Brunbjerg, A.K., H.H. Bruun, L. Dalby, A.T. Classen, C. Fløjgaard, T.G. Frøslev, O.L.P. Hansen, T.T. Høye, et al. 2020. Multi-taxon inventory reveals highly consistent biodiversity responses to ecospace variation. Oikos 129: 1381–1392.
Brunbjerg, A.K., H.H. Bruun, L. Dalby, C. Fløjgaard, T.G. Frøslev, T.T. Høye, I. Goldberg, T. Læssøe, et al. 2018. Vascular plant species richness and bioindication predict multi-taxon species richness. Methods in Ecology and Evolution 9: 2372–2382.
Brussaard, L., P.C. De Ruiter, and G.G. Brown. 2007. Soil biodiversity for agricultural sustainability. Agriculture, Ecosystems & Environment 121: 233–244.
Chivenge, P.P., H.K. Murwira, K.E. Giller, P. Mapfumo, and J. Six. 2007. Long-term impact of reduced tillage and residue management on soil carbon stabilization: Implications for conservation agriculture on contrasting soils. Soil and Tillage Research 94: 328–337.
Coulibaly, S.F., V. Coudrain, M. Hedde, N. Brunet, B. Mary, S. Recous, and M. Chauvat. 2017. Effect of different crop management practices on soil Collembola assemblages: A 4-year follow-up. Applied Soil Ecology 119: 354–366.
de Graaff, M.A., N. Hornslein, H.L. Throop, P. Kardol, and L.T. van Diepen. 2019. Effects of agricultural intensification on soil biodiversity and implications for ecosystem functioning: A meta-analysis. Advances in Agronomy 155: 1–44.
Degrune, F., N. Theodorakopoulos, M. Dufrêne, G. Colinet, B. Bodson, M.P. Hiel, B. Taminiau, C. Nezer, et al. 2016. No favorable effect of reduced tillage on microbial community diversity in a silty loam soil (Belgium). Agriculture, Ecosystems & Environment 224: 12–21.
Derpsch, R., T. Friedrich, A. Kassam, and H. Li. 2010. Current status of adoption of no-till farming in the world and some of its main benefits. International Journal of Agricultural and Biological Engineering 3: 1–25.
D’Hose, T., L. Molendijk, L. Van Vooren, W. van den Berg, H. Hoek, W. Runia, F. van Evert, H. ten Berg, et al. 2018. Responses of soil biota to non-inversion tillage and organic amendments: An analysis on European multiyear field experiments. Pedobiologia 66: 18–28.
Ejrnæs, R., H.H. Bruun, and B.J. Graae. 2006. Community assembly in experimental grasslands: Suitable environment or timely arrival? Ecology 87: 1225–1233.
Ejrnæs, R., T.G. Frøslev, T.T. Høye, R. Kjøller, A. Oddershede, A.K. Brunbjerg, A.J. Hansen, and H.H. Bruun. 2018. Uniquity: A general metric for biotic uniqueness of sites. Biological Conservation 225: 98–105.
Ejrnæs, R., P. Wiberg-Larsen, T.E. Holm, A. Josefson, B. Strandberg, B. Nygaard, L.W. Andersen, A. Winding, et al. 2011. Danmarks biodiversitet 2010—Status, udvikling og trusler. Faglig rapport fra DMU nr. 815. Danmarks Miljøundersøgelser, Aarhus Universitet. Aarhus, Denmark (in Danish) (Report)
Fløjgaard, C., T.G. Frøslev, A.K. Brunbjerg, H.H. Bruun, J. Moeslund, A.J. Hansen, and R. Ejrnæs. 2019. Predicting provenance of forensic soil samples: Linking soil to ecological habitats by metabarcoding and supervised classification. PLoS ONE 14: e0202844.
Fredshavn, J.R., B. Nygaard, R. Ejrnæs, C. Damgaard, O.R. Therkildsen, M. Elmeros, P. Wind, L.S. Johansson, et al. 2019. Bevaringsstatus for naturtyper og arter—2019: Habitatdirektivets Artikel 17-rapportering. Aarhus, Denmark (in Danish) (Report)
Frøslev, T.G., R. Kjøller, H.H. Bruun, R. Ejrnæs, A.K. Brunbjerg, C. Pietroni, and A.J. Hansen. 2017. Algorithm for post-clustering curation of DNA amplicon data yields reliable biodiversity estimates. Nature Communications 8: 1–11.
Frøslev, T.G., R. Kjøller, H.H. Bruun, R. Ejrnæs, A.J. Hansen, T. Læssøe, and J. Heilmann-Clausen. 2019. Man against machine: Do fungal fruitbodies and eDNA give similar biodiversity assessments across broad environmental gradients? Biological Conservation 233: 201–212.
Grime, J.P. 1974. Vegetation classification by reference to strategies. Nature 250: 26–31.
Huston, M. 1979. A general hypothesis of species diversity. The American Naturalist 113: 81–101.
Jurburg, S.D., I. Nunes, A. Brejnrod, S. Jacquiod, A. Priemé, S.J. Sørensen, J.D. Van Elsas, and J.F. Salles. 2017. Legacy effects on the recovery of soil bacterial communities from extreme temperature perturbation. Frontiers in Microbiology 8: 1832.
Kuhwald, M., M. Blaschek, J. Brunotte, and R. Duttmann. 2017. Comparing soil physical properties from continuous conventional tillage with long-term reduced tillage affected by one-time inversion. Soil Use and Management 33: 611–619.
Le Guillou, C., N. Chemidlin Prévost-Bouré, B. Karimi, N. Akkal-Corfini, S. Dequiedt, V. Nowak, S. Terrat, S. Menasseri-Aubry, et al. 2019. Tillage intensity and pasture in rotation effectively shape soil microbial communities at a landscape scale. MicrobiologyOpen 8: e00676.
Legrand, F., A. Picot, J. F. Cobo-Díaz, M. Carof, W. Chen, and G. Le Floch. 2018. Effect of tillage and static abiotic soil properties on microbial diversity. Applied Soil Ecology 132: 135–145.
López-Garrido, R., E. Madejón, M. León-Camacho, I. Girón, F. Moreno, and J.M. Murillo. 2014. Reduced tillage as an alternative to no-tillage under Mediterranean conditions: A case study. Soil and Tillage Research 140: 40–47.
Meisner, A., A. Leizeaga, J. Rousk, and E. Bååth. 2017. Partial drying accelerates bacterial growth recovery to rewetting. Soil Biology and Biochemistry 112: 269–276.
Moos, J.H., S. Schrader, H.M. Paulsen, and G. Rahmann. 2016. Occasional reduced tillage in organic farming can promote earthworm performance and resource efficiency. Applied Soil Ecology 103: 22–30.
Newbold, T., L.N. Hudson, S.L.L. Hill, S. Contu, I. Lysenko, R.A. Senior, L. Börger, D.J. Bennet, et al. 2015. Global effects of land use on local terrestrial biodiversity. Nature 520: 45–50.
Paoletti, M.G., D. Pimentel, B.R. Stinner, and D. Stinner. 1992. Agroecosystem biodiversity: Matching production and conservation biology. Agriculture, Ecosystems & Environment 40: 3–23.
Phalan, B., M. Onial, A. Balmford, and R.E. Green. 2011. Reconciling food production and biodiversity conservation: Land sharing and land sparing compared. Science 333: 1289–1291.
Sengupta, A., and W.A. Dick. 2015. Bacterial community diversity in soil under two tillage practices as determined by pyrosequencing. Microbial Ecology 70: 853–859.
Strickland, M.S., M.A. Callaham Jr., E.S. Gardiner, J.A. Stanturf, J.W. Leff, N. Fierer, and M.A. Bradford. 2017. Response of soil microbial community composition and function to a bottomland forest restoration intensity gradient. Applied Soil Ecology 119: 317–326.
Taylor, S.J., B.S. Evans, E.P. White, and A.H. Hurlbert. 2018. The prevalence and impact of transient species in ecological communities. Ecology 99: 1825–1835.
Tsiafouli, M.A., E. Thébault, S.P. Sgardelis, P.C. De Ruiter, W.H. Van Der Putten, K. Birkhofer, L. Hemerik, F.T. de Vries, et al. 2015. Intensive agriculture reduces soil biodiversity across Europe. Global Change Biology 21: 973–985.
Tuck, S.L., C. Winqvist, F. Mota, J. Ahnström, L.A. Turnbull, and J. Bengtsson. 2014. Land-use intensity and the effects of organic farming on biodiversity: A hierarchical meta-analysis. Journal of Applied Ecology 51: 746–755.
Turley, N.E., L. Bell-Dereske, S.E. Evans, and L.A. Brudvig. 2020. Agricultural land-use history and restoration impact soil microbial biodiversity. Journal of Applied Ecology 57 (5): 852–863.
Veresoglou, S.D., J.M. Halley, and M.C. Rillig. 2015. Extinction risk of soil biota. Nature Communications 6: 1–10.
Zandersen, M., S.L. Jørgensen, D. Nainggolan, S. Gyldenkærne, A. Winding, M.H. Greve, and M. Termansen. 2016. Potential and economic efficiency of using reduced tillage to mitigate climate effects in Danish agriculture. Ecological Economics 123: 14–22.
Acknowledgements
Henrik Kruse Rasmussen (Agrovi) is acknowledged for contributing with information and selection of the investigated sites. The Aage V. Jensen Foundation is thanked for generous financial support to the project DNAmark and15 Juni Fonden for support to the study, through a grant to Kristian Thorup-Kristensen.
Funding
The work was supported financially by a Grant from The Aage V. Jensen Foundation to the project DNAmark, and by a Grant from 15 Juni Fonden to Kristian Thorup-Kristensen.
Author information
Authors and Affiliations
Contributions
RE and TGF designed the study, planned the analyses, and lead the writing of the paper. IBN, SS and TGF carried out the field work. IBN did the laboratory work. TGF performed the bioinformatic and statistical analyses. All authors contributed to writing and revising the paper.
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Frøslev, T.G., Nielsen, I.B., Santos, S.S. et al. The biodiversity effect of reduced tillage on soil microbiota. Ambio 51, 1022–1033 (2022). https://doi.org/10.1007/s13280-021-01611-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13280-021-01611-0