Plant-soil feedback (PSF) effects are studied as plant growth responses to soil previously conditioned by another plant. These studies usually exclude effects of soil fauna, such as nematodes, soil arthropods, and earthworms, although these organisms are known to influence plant performance. Here, we aimed to explore effects of a model microarthropod community on PSFs. We performed a PSF experiment in microcosms with two plant species, Phleum pratense and Poa pratensis. We added a model microarthropod community consisting of three fungivorous springtail species (Proisotoma minuta, Folsomia candida, and Sinella curviseta) and a predatory mite (Hypoaspis aculeifer) to half of the microcosms. We measured seedling establishment and plant biomass, nematode and microbial community composition, microbial biomass, and mycorrhizal colonization of roots. Microarthropods caused changes in the composition of nematode and microbial communities. Their effect was particularly strong in Phleum plants where they altered the composition of bacterial communities. Microarthropods also generally influenced plant performance, and their effects depended on previous soil conditioning and the identity of plant species. Microarthropods did not affect soil microbial biomass and mycorrhizal colonization of roots. We conclude that the role of soil microarthropods should be considered in future PSF experiments, especially as their effects are plant species-specific.

Department of Botany Faculty of Science Charles University Prague Benátská 2 128 01 Praha 2 Czech Republic

Friedrich Schiller University of Jena Institute of Ecology Dornburger Str 159 07743 Jena Germany

German Centre for Integrative Biodiversity Research Halle Jena Leipzig Deutscher Platz 5e 04103 Leipzig Germany

Institute of Biology Leipzig University Deutscher Platz 5e 04103 Leipzig Germany

Institute of Botany Czech Academy of Sciences v v i Zámek 1 252 43 Průhonice Czech Republic

See more in PubMed

Bever JD. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol. 2003;157:465–473. doi: 10.1046/j.1469-8137.2003.00714.x. PubMed DOI

van der Putten WH, et al. Plant-soil feedbacks: the past, the present and future challenges. J. Ecol. 2013;101:265–276. doi: 10.1111/1365-2745.12054. DOI

Bever JD, Westover KM, Antonovics J. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J. Ecol. 1997;85:561–573. doi: 10.2307/2960528. DOI

Ehrenfeld JG, Ravit B, Elgersma K. Feedback in the plant-soil system. Annu. Rev. Environ. Resour. 2005;30:75–115. doi: 10.1146/annurev.energy.30.050504.144212. DOI

Brinkman EP, V der Putten WH, Bakker EJ, Verhoeven KJF. Plant-soil feedback: Experimental approaches, statistical analyses and ecological interpretations. J. Ecol. 2010;98:1063–1073. doi: 10.1111/j.1365-2745.2010.01695.x. DOI

Bever J. Feeback between plants and their soil communities in an old field community. Ecology. 1994;75:1965–1977. doi: 10.2307/1941601. DOI

Klironomos JN. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature. 2002;417:67–70. doi: 10.1038/417067a. PubMed DOI

Hawkes CV, Kivlin SN, Du J, Eviner VT. The temporal development and additivity of plant-soil feedback in perennial grasses. Plant Soil. 2013;369:141–150. doi: 10.1007/s11104-012-1557-0. DOI

Dostálek T, Münzbergová Z, Kladivová A, Macel M. Plant–soil feedback in native vs. invasive populations of a range expanding plant. Plant Soil. 2016;399:209–220. doi: 10.1007/s11104-015-2688-x. DOI

de Rooij-van der Goes PCEM, van Dijk C, van der Putten WH, Jungerius PD. Effects of sand movement by wind on nematodes and soil-borne fungi in coastal foredunes. J. Coast. Conserv. 1997;3:133–142. doi: 10.1007/BF02905239. DOI

Bonkowski M, Villenave C, Griffiths B. Rhizosphere fauna: The functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant Soil. 2009;321:213–233. doi: 10.1007/s11104-009-0013-2. DOI

Wardle Da, et al. Ecological linkages between aboveground and belowground biota. Science. 2004;304:1629–1633. doi: 10.1126/science.1094875. PubMed DOI

Klironomos JN, Ursic M. Density-dependent grazing on the extraradical hyphal network of the arbuscular mycorrhizal fungus, Glomus intraradices, by the collembolan, Folsomia candida. Biol. Fertil. Soils. 1998;26:250–253. doi: 10.1007/s003740050375. DOI

Gange A. Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends Ecol. Evol. 2000;15:369–372. doi: 10.1016/S0169-5347(00)01940-6. PubMed DOI

Sabatini MA, Innocenti G. Effects of collembola on plant-pathogenic fungus interactions in simple experimental systems. Biol. Fertil. Soils. 2001;33:62–66. doi: 10.1007/s003740000290. DOI

Schreiner RP, Bethlenfalvay GJ. Crop residue and Collembola interact to determine the growth of mycorrhizal pea plants. Biol. Fertil. Soils. 2003;39:1–8. doi: 10.1007/s00374-003-0672-8. DOI

Maboreke HR, et al. Multitrophic interactions in the rhizosphere of a temperate forest tree affect plant carbon flow into the belowground food web. Soil Biol. Biochem. 2017;115:526–536. doi: 10.1016/j.soilbio.2017.09.002. DOI

Kuzyakov Y, Xu X. Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol. 2013;198:656–669. doi: 10.1111/nph.12235. PubMed DOI

Maire N, Borcard D, Laczkó E, Matthey W. Organic matter cycling in grassland soils of the Swiss Jura mountains: Biodiversity and strategies of the living communities. Soil Biol. Biochem. 1999;31:1281–1293. doi: 10.1016/S0038-0717(99)00043-7. DOI

Filser J. The role of Collembola in carbon and nitrogen cycling in soil. Pedobiologia (Jena). 2002;46:234–245.

Ngosong C, Gabriel E, Ruess L. Collembola grazing on arbuscular mycorrhiza fungi modulates nutrient allocation in plants. Pedobiologia - J. Soil Ecol. 2014;57:171–179. doi: 10.1016/j.pedobi.2014.03.002. DOI

Setala H, Huhta V. Soil fauna increase Betula pendula growth: laboratory experiments with coniferous forest floor. Ecology. 1991;72:665–671. doi: 10.2307/2937206. DOI

Bradford MA, et al. Impacts of soil faunal community composition on model grassland ecosystems. Science (80-.). 2002;298:615–618. doi: 10.1126/science.1075805. PubMed DOI

De Deyn GB, et al. Soil invertebrate fauna enhances grassland succession and diversity. Nature. 2003;422:711–713. doi: 10.1038/nature01548. PubMed DOI

Eisenhauer N, et al. Impact of above- and below-ground invertebrates on temporal and spatial stability of grassland of different diversity. J. Ecol. 2011;99:572–582.

Cortois, R., Schröder-Georgi, T., Weigelt, A., van der Putten, W. H. & De Deyn, G. B. Plant-soil feedbacks: role of plant functional group and plant traits. J. Ecol. (2016).

Münzbergová Z, Šurinová M. The importance of species phylogenetic relationships and species traits for the intensity of plant-soil feedback. Ecosphere. 2015;6:234. doi: 10.1890/ES15-00206.1. DOI

Yang Q, et al. Plant–soil biota interactions of an invasive species in its native and introduced ranges: Implications for invasion success. Soil Biol. Biochem. 2013;65:78–85. doi: 10.1016/j.soilbio.2013.05.004. DOI

Agrios, G. N. Plant pathology. (Academic Press, 2005).

Zelmer CD, Cuthbertson L, Currah RS. Fungi associated with terrestrial orchid mycorrhizas, seeds and protocorms. Mycoscience. 1996;37:439–448. doi: 10.1007/BF02461001. DOI

McKendrick SL, Leake JR, Taylor DL, Read DJ. Symbiotic germination and development of myco-heterotrophic plants in nature: ontogeny of Corallorhiza trifida and characterization of its mycorrhizal fungi. New Phytol. 2000;145:523–537. doi: 10.1046/j.1469-8137.2000.00603.x. PubMed DOI

Westover KM, Kennedy ANNC, Kelley SE. Patterns of Rhizosphere Microbial Community Structure Associated with Co-Occurring Plant Species. J. Ecol. 1997;85:863–873. doi: 10.2307/2960607. DOI

Marschner P, Yang C-H, Lieberei R, Crowley DE. Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol. Biochem. 2001;33:1437–1445. doi: 10.1016/S0038-0717(01)00052-9. DOI

Klironomos JN. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature. 2002;417:67–70. doi: 10.1038/417067a. PubMed DOI

Vries FTD, Shade A. Controls on soil microbial community stability under climate change. Front. Microbiol. 2013;4:269. doi: 10.3389/fmicb.2013.00265. PubMed DOI PMC

Jousset A, Eisenhauer N, Materne E, Scheu S. Evolutionary history predicts the stability of cooperation in microbial communities. Nat. Commun. 2013;4:2573. doi: 10.1038/ncomms3573. PubMed DOI

Bongers T, Bongers M. Functional diversity of nematodes. Appl. Soil Ecol. 1998;10:239–251. doi: 10.1016/S0929-1393(98)00123-1. DOI

Griffiths BS, Bonkowski M, Dobson G, Caul S. Changes in soil microbial community structure in the presence of microbial-feeding nematodes and protozoa. Pedobiologia (Jena). 1999;43:297–304.

Bonkowski M, Cheng WX, Griffiths BS, Alphei G, Scheu S. Microbial-faunal interactions in the rhizosphere and effects on plant growth. Eur. J. Soil Biol. 2000;36:135–147. doi: 10.1016/S1164-5563(00)01059-1. DOI

Endlweber K, Ruess L, Scheu S. Collembola switch diet in presence of plant roots thereby functioning as herbivores. Soil Biol. Biochem. 2009;41:1151–1154. doi: 10.1016/j.soilbio.2009.02.022. DOI

Mitschunas N, Wagner M, Filser J. Evidence for a positive influence of fungivorous soil invertebrates on the seed bank persistence of grassland species. J. Ecol. 2006;94:791–800. doi: 10.1111/j.1365-2745.2006.01146.x. DOI

Mitschunas N, Wagner M, Filser J. Increased field emergence of seedlings at high densities of fungivorous soil mesofauna. J. Torrey Bot. Soc. 2008;135:272–280. doi: 10.3159/08-RA-022.1. DOI

Nietschke L, Burfeindt I, Seupt A, Filser J. Collembola and seed germination: relevance of substrate quality and evidence for seed attack. Soil Org. 2011;83:451–462.

Glimskar A, Ericsson T. Relative nitrogen limitation at steady-state nutrition as a determinant of plasticity in five grassland plant species. Ann. Bot. 1999;84:413–420. doi: 10.1006/anbo.1999.0929. DOI

Müller I, Schmid B, Weiner J. The effect of nutrient availability on biomass allocation patterns in 27 species of herbaceous plants. Perspect. Plant Ecol. Evol. Syst. 2000;3:115–127. doi: 10.1078/1433-8319-00007. DOI

Cambui CA, et al. Patterns of plant biomass partitioning depend on Nitrogen source. PLoS One. 2011;6:1–7. doi: 10.1371/journal.pone.0019211. PubMed DOI PMC

Heckmann LH, Ruf A, Nienstedt KM, Krogh PH. Reproductive performance of the generalist predator Hypoaspis aculeifer (Acari: Gamasida) when foraging on different invertebrate prey. Appl. Soil Ecol. 2007;36:130–135. doi: 10.1016/j.apsoil.2007.01.002. DOI

Rusek J. Biodiversity of Collembola and their functional role in the ecosystem. Biodivers. Conserv. 1998;7:1207–1219. doi: 10.1023/A:1008887817883. DOI

Hopkin, S. P. Biology of the Springtails (Insecta: Collembola). (Oxford University Press, 1997).

Sabais ACW, Scheu S, Eisenhauer N. Plant species richness drives the density and diversity of Collembola in temperate grassland. Acta Oecologica. 2011;37:195–202. doi: 10.1016/j.actao.2011.02.002. DOI

Thakur MP, et al. Cascading effects of belowground predators on plant communities are density-dependent. Ecol. Evol. 2015;5:4300–4314. doi: 10.1002/ece3.1597. PubMed DOI PMC

Kulmatiski A, Beard KH, Stevens JR, Cobbold SM. Plant-soil feedbacks: a meta-analytical review. Ecol. Lett. 2008;11:980–92. doi: 10.1111/j.1461-0248.2008.01209.x. PubMed DOI

Roscher C, Schumacher J, Baade J. The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community. Basic Appl. Ecol. 2004;121:107–121. doi: 10.1078/1439-1791-00216. DOI

Cahill, J. F. et al. No silver bullet: Different soil handling techniques are useful for different research questions, exhibit differential type I and II error rates, and are sensitive to sampling intensity. New Phytol. 11–14 (2016). PubMed

Eisenhauer N, et al. Impacts of earthworms and arbuscular mycorrhizal fungi (Glomus intraradices) on plant performance are not interrelated. Soil Biol. Biochem. 2009;41:561–567. doi: 10.1016/j.soilbio.2008.12.017. DOI

Eisenhauer N, Sabais ACW, Scheu S. Collembola species composition and diversity effects on ecosystem functioning vary with plant functional group identity. Soil Biol. Biochem. 2011;43:1697–1704. doi: 10.1016/j.soilbio.2011.04.015. DOI

Sabais ACW, et al. Soil organisms shape the competition between grassland plant species. Oecologia. 2012;170:1021–1032. doi: 10.1007/s00442-012-2375-z. PubMed DOI

Eisenhauer N, Sabais ACW, Scheu S. Collembola species composition and diversity effects on ecosystem functioning vary with plant functional group identity. Soil Biol. Biochem. 2011;43:1697–1704. doi: 10.1016/j.soilbio.2011.04.015. DOI

Ruess L, Chamberlain PM. The fat that matters: Soil food web analysis using fatty acids and their carbon stable isotope signature. Soil Biol. Biochem. 2010;42:1898–1910. doi: 10.1016/j.soilbio.2010.07.020. DOI

Frostegård Å, Tunlid A, Bååth E. Use and misuse of PLFA measurements in soils. Soil Biol. Biochem. 2011;43:1621–1625. doi: 10.1016/j.soilbio.2010.11.021. DOI

Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959;37:911–917. doi: 10.1139/y59-099. PubMed DOI

Ruess L. Studies on the nematode fauna of an acid forest soil: spatial distribution and extraction. Nematology. 1995;41:229–239. doi: 10.1163/003925995X00198. DOI

Nijs D. PM 7/119 (1) Nematode extraction. EPPO Bull. 2013;43:471–495. doi: 10.1111/epp.12077. DOI

Bongers, T. De Nematoden van Nederland. (KNNV Publishing, 1994).

Yeates GW, Bongers T, de Goede RGM, Freckman DW, Georgieva SS. Feeding habits in soil nematode families and genera – an outline for soil ecologists. J. Nematol. 1993;25:315–331. PubMed PMC

Scheu S. Automated measurement of the respiratory response of soil microcompartments: active microbial biomass in earthworm faeces. Soil Biol. Biochem. 1992;24:1–6. doi: 10.1016/0038-0717(92)90235-P. DOI

Beck T, et al. An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biol. Biochem. 1997;29:1023–1032. doi: 10.1016/S0038-0717(97)00030-8. DOI

Giovannetti M, Mosse B. An evaluation of techniques for measuring vesicular mycorrhizal infection in roots. New Phytologist. 1980;84:489–500. doi: 10.1111/j.1469-8137.1980.tb04556.x. DOI

R Development Core Team. R: A language and environment for statistical computing (2017).

Lepš, J. & Šmilauer, P. Multivariate Analysis of Ecological Data using CANOCO, (Cambridge University Press 2003).

TerBraak, C. J. & Šmilauer, P. Canoco reference manual and user’s guide: software for ordination, version 5.0. (2012).