Disturbances are intrinsic drivers of structure and function in ecosystems, hence predicting their effects in forest ecosystems is essential for forest conservation and/or management practices. Yet, knowledge regarding belowground impacts of disturbance events still remains little understood and can greatly vary by taxonomic and functional identity, disturbance type and local environmental conditions. To address this gap in knowledge, we conducted a survey of soil-dwelling Protura, across forests subjected to different disturbance regimes (i.e. windstorms, insect pest outbreaks and clear-cut logging). We expected that the soil proturan assemblages would differ among disturbance regimes. We also hypothesized that these differences would be driven primarily by variation in soil physicochemical properties thus the impacts of forest disturbances would be indirect and related to changes in food resources. To verify that sampling included two geographically distant subalpine glacial lake catchments that differed in underlying geology, each having four different types of forest disturbance, i.e. control, bark beetle outbreak (BB), windthrow + BB (wind + BB) and clear-cut. As expected, forest disturbance had negative effects on proturan diversity and abundance, with multiple disturbances having the greatest impacts. However, differences in edaphic factors constituted a stronger driver of variability in distribution and abundance of proturans assemblages. These results imply that soil biogeochemistry and resource availability can have much stronger effects on proturan assemblages than forest disturbances.

Biology Centre of the Czech Academy of Sciences Institute of Hydrobiology Na Sádkách 7 370 05 České Budějovice Czech Republic

Biology Centre of the Czech Academy of Sciences Institute of Soil Biology Na Sádkách 7 370 05 České Budějovice Czech Republic

Institute of Nature Conservation Polish Academy of Sciences Mickiewicza 33 31 120 Kraków Poland

Institute of Systematics and Evolution of Animals Polish Academy of Sciences Sławkowska 17 31 016 Krakow Poland

Museum and Institute of Zoology Polish Academy of Sciences Wilcza 64 00 679 Warsaw Poland

State Museum of Natural History Ukrainian Academy of Sciences Teatral'na 18 UA 79008 L'viv Ukraine

Zobrazit více v PubMed

Fischer A, Marshall P, Camp A. Disturbances in deciduous temperate forest ecosystems of the northern hemisphere: their effects on both recent and future forest development. Biodivers. Conserv. 2013;22:1863–1893. doi: 10.1007/s10531-013-0525-1. DOI

Frelich L. E. Forest dynamics and disturbance regimes. (Cambridge, Cambridge University Press, 2002).

Seidl R, Schelhaas M-J, Rammer W, Verkerk PJ. Increasing forest disturbances in Europe and their impact on carbon storage. Nat. Clim. Change. 2014;4:806–810. doi: 10.1038/nclimate2318. PubMed DOI PMC

Thon D, Seidl R. Natural disturbance impacts on ecosystem services and biodiversity in temperate and boreal forests. Bio. Rev. 2016;91:760–781. doi: 10.1111/brv.12193. PubMed DOI PMC

Turner MG. Disturbance and landscape dynamics in a changing world. Ecology. 2010;91:2833–2849. doi: 10.1890/10-0097.1. PubMed DOI

Bonan GB. Forests and climate change: forcing, feedbacks and the climate benefits of forests. Science. 2008;320:1444–1449. doi: 10.1126/science.1155121. PubMed DOI

Lukac M. Soil biodiversity and environmental change in European forests. Cent. Eur. For. J. 2017;63:59–65.

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

Hättenschwiler S, Tiunov AV, Scheu S. Biodiversity and litter decomposition in terrestrial ecosystems. Ann. Rev. Ecol. Evol. Syst. 2005;36:191–218. doi: 10.1146/annurev.ecolsys.36.112904.151932. DOI

Lavelle, P., Lattaud, C., Trigo, D. & Barois, I. Mutualism and biodiversity in soils in The Significance and Regulation of Soil Biodiversity (eds. Collins, H. P., Robertson, G. P. & Klug, M. J.) 23–33 (Kluwer Academic Publishers, Dordrecht, 1995).

Grandy AS, Wieder WR, Wickings K, Kyker-Snowman E. Beyond microbes: Are fauna the next frontier in soil biogeochemical models? Soil Biol. Biochem. 2016;102:40–44. doi: 10.1016/j.soilbio.2016.08.008. DOI

Rusek J. Soil microstructures-contributions on specific soil organisms. Quaest. Entomol. 1985;21:497–514.

Thorn S, Bässler C, Svoboda M, Müller J. Effects of natural disturbances and salvage logging on biodieversity – lessons from the Bohemian Forest. Forest Ecol. Manag. 2016;385:113–118.

Coleman, D. C., Callaham, M. A. Jr. & Crossley, D. A. Jr. Fundamentals of Soil Ecology, third edition, (London, Elsevier Academic Press, 2018).

Bastida F, Zsolnay A, Hernández T, García C. Past, present and future of soil quality indices: A biological perspective. Geoderma. 2008;147:159–171. doi: 10.1016/j.geoderma.2008.08.007. DOI

Marshall VG. Impacts of forest harvesting on biological processes in northern forest soils. Forest Ecol. Manag. 2000;133:43–60. doi: 10.1016/S0378-1127(99)00297-2. DOI

Coyle DR, et al. Soil fauna responses to natural disturbances, invasive species, and global climate change: current state of the science and call to action. Soil Biol. Biochem. 2017;110:116–133. doi: 10.1016/j.soilbio.2017.03.008. DOI

Lisa C, et al. Impact of wildfire on the edaphic microarthropod community in a Pinus pinaster forest in central Italy. iForest. 2015;8:874–883. doi: 10.3832/ifor1404-008. DOI

Sterzyńska M, Skłodowski J. Divergence of soil microarthropod (Hexapoda: Collembola) recovery patterns during natural regeneration and regeneration by planting of windthrow pine forests. Forest Ecol. Manag. 2018;429:414–424. doi: 10.1016/j.foreco.2018.07.033. DOI

Farská J, Starý J, Rusek J. Soil microarthropods in non-intervention montane spruce forest regenerating after bark-beetle outbreak. Ecol. Res. 2014;29:1087–1096. doi: 10.1007/s11284-014-1197-3. DOI

Nosek J. Niches of Protura in biogeocoenoses. Pedobiologia. 1975;15:257–265.

Stumpp J. Zur Ökologie einheimischer Proturen (Arthropoda: Insecta) in Fichtenforsten. Zool. Beitr. 1990;33:335–432.

Bluhm SL, et al. Protura are unique: First evidence of specialized feeding on ectomycorrhizal fungi in soil invertebrates. BMC Ecology. 2019;19:10. doi: 10.1186/s12898-019-0227-y. PubMed DOI PMC

Shrubovych J, Sterzyńska M. Diversity and distributional pattern of soil microarthropods (Protura) across a transitional zone in Ukraine. Can. Entomol. 2017;50:628–638. doi: 10.4039/tce.2017.30. DOI

Sterzyńska M, Orlov O, Shrubovych J. Effect of hydrologic disturbance regimes on Protura variability in a river floodplain. Ann. Zool. Fenn. 2012;49:309–320. doi: 10.5735/086.049.0504. DOI

Kaňa J, Kopáček J, Tahovská K, Šantrůčková H. Tree dieback and related changes in nitrogen dynamics modify the concentration and proportions of cations on soil sorption complex. Ecol. Indic. 2019;97:319–328. doi: 10.1016/j.ecolind.2018.10.032. DOI

Kopáček J, Vrba J. Integrated ecological research of catchment–lake ecosystems in the Bohemian Forest (Central Europe): A preface. Biologia. 2006;61:363–370.

Cottle, R. Linking Geology and Biodiversity, English Nature Research Reports. Report562, (English Nature, Northminster House, Peterborough PE1 1UA, 2004).

Hahm WJ, Riebe CS, Lukens CE, Araki S. Bedrock composition regulates mountain ecosystems and landscape evolution. PNAS. 2014;111:3338–3343. doi: 10.1073/pnas.1315667111. PubMed DOI PMC

Šantrůčková H, Vrba J, Picek T, Kopáček J. Soil biochemical activity and phosphorus transformations and losses from acidified forest soils. Soil Biol. Biochem. 2004;36:1569–1576. doi: 10.1016/j.soilbio.2004.07.015. DOI

Pánek, T. & Hradecký, J. Landscapes and Landforms of the Czech Republic. (Switzerland, Springer, 2016).

Šantrůčková, H. et. al. About mountain spruces from the Bohemian Forest. A guide to the national parks’ forest ecosystems. (Faculty of Science, University of South Bohemia and Czech Society for Ecology, Vimperk, 2010).

Kopáček J, Brzakova M, Hejzlar J, Porcal P, Vrba J. Nutrient cycling in a strongly acidified mesotrophic lake. Limnol. Oceanogr. 2004;49(4):1202–1213. doi: 10.4319/lo.2004.49.4.1202. DOI

Kopáček J, et al. Physical, chemical, and biochemical characteristics of soils in watersheds of the Bohemian Forest lakes: I. Plešné Lake. Silva Gabreta. 2002;8:43–66.

Kopáček J, et al. Physical, chemical, and biochemical characteristics of soils in watersheds of the Bohemian Forest lakes: II. Čertovo and Černé Lakes. Silva Gabreta. 2002;8:63–64.

Nosek, J. The European Protura. Their taxonomy, ecology and distribution. With keys for determination, (Muséum d’Histoire Naturelle, Genève, 1973).

Shrubovych J, Bartel D, Szucsich NU, Resch MC, Pass G. Morphological and genetic analysis of the Acerentomon doderoi group (Protura: Acerentomidae) with description of A. christiani sp. nov. PLoS ONE. 2016;11:e0148033. doi: 10.1371/journal.pone.0148033. PubMed DOI PMC

Galli L, Shrubovych J, Bu Y, Zinni M. Genera of the Protura of the World: diagnosis, distribution, and key. ZooKeys. 2018;772:1–45. doi: 10.3897/zookeys.772.24410. PubMed DOI PMC

Shrubovych J, Bernard EC. A key for the determination of European species of Eosentomon Berlese, 1909 (Protura: Eosentomata: Eosentomidae) ZooKeys. 2018;742:1–12. doi: 10.3897/zookeys.742.22664. PubMed DOI PMC

Kopáček J, Hejzlar J. Semi-micro determination of total phosphorus in fresh waters with perchloric acid digestion. Int. J. Environ. Anal. Chem. 1993;53:173–183. doi: 10.1080/03067319308045987. DOI

Thomas, G. Exchangeable cations in Methods of Soil Analysis, Part 2, 2nd (eds. Page, A. L., Miller, R. H. & Keeney, D. R.) 159–166 (America Society of Agronomy and Soil Science of America, Madison WI, 1982).

Wardle DA. A comparative assessment of the factors which influence microbial biomass carbon and nitrogen levels in soil. Biol. Rev. 1992;67:321–358. doi: 10.1111/j.1469-185X.1992.tb00728.x. DOI

Nouri E, Breullin-Sessoms F, Feller U, Reinhardt D. Phosphorous and nitrogen regulate Arbuscular Mycorrhizal Symbiosis in Petunia hybrid. PLoS ONE. 2014;9(3):e908451. doi: 10.1371/journal.pone.0090841. PubMed DOI PMC

Pinheiro, J., Bates, D., DebRoy, S. & Sarker, D, Core Team R nlm: Linear and Nonlinear Mixed Effects Models. R package version 3.1-13. http://CRAN.Rproject.org/package=nlme (2017).

Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. ImerTest: Tests for Random and Fixed Effects for Linear Mixed Effect Models (Imer Objects of lme4 Package), R Package Version 2.0-6. http://cran.r-project.org/package=lmerTest (2014).

Lepš, J. & Šmilauer, P. Multivariate analysis of ecological data using CANOCO. (Cambridge University Press, Cambridge, UK, 2003).

ter Braak, C. J. F & Šmilauer, P. Canoco reference manual and user’s guide: software for ordination (version 5.0). (Microcomputer Power, Ithaca, Ny, USA, 2012).

Šmilauer, P. & Jan Lepš, J. Multivariate Analysis of Ecological Data using CANOCO 5, 2nd edition. (Cambridge University Press, 2014).

Core Team, R. R. A Language and Environment for Statistical Computing. https://www.R-project.org/ (2016).

Teh YA, Silver VL, Scatena F. A decade of belowground reorganization following multiple disturbances in a subtropical wet forest. Plant Soil. 2009;323:197–212. doi: 10.1007/s11104-009-9926-z. DOI

Mills, C. G., Allen, R. J. & Blythe, R. A. Resource spectrum engineering by specialist species can shit the specialist-generalist balance. Theor. Ecol. 10.1007/s12080-019-00436-8 (2019).

Platt WJ, Connell JH. Natural disturbances and directional replacement of species. Ecol. Monogr. 2003;73(4):507–522. doi: 10.1890/01-0552. DOI

Clavel J, Juliard R, Devictor V. Worldwide decline of specialist species: toward a global functional homogenization? Front. Ecol. Environ. 2011;9:222–228. doi: 10.1890/080216. DOI

Bakker MR, et al. Belowground biodiversity relates positively to ecosystem services of European forests. Front. For. Glob. Change. 2019;2:6. doi: 10.3389/ffgc.2019.00006. DOI

Setälä H, Haimi J, Siira-Pietikäinen A. Sensitivity of soil processes in northern forest soils: are management practices a treat? Forest Ecol. Manag. 2000;133:5–11. doi: 10.1016/S0378-1127(99)00293-5. DOI

Pollierer MM, Scheu S. Driving factors and temporal fluctuation of Collembola communities and reproductive mode across forest types and regions. Ecol. Evol. 2017;7:4390–4403. doi: 10.1002/ece3.3035. PubMed DOI PMC

Cox F. Nitrogen availability is a primary determinant of confer mycorrhizas across complex environmental gradients. Ecol. Lett. 2010;13:1103–1113. doi: 10.1111/j.1461-0248.2010.01494.x. PubMed DOI

Wang Q, et al. Effects of nitrogen and phosphorous inputs on soil bacterial abundance, diversity, and community composition in Chinese Fir plantations. Front. Microbiol. 2018;9:1543. doi: 10.3389/fmicb.2018.01543. PubMed DOI PMC

Smykla J, et al. Geochemical and biotic factors influencing diversity and distribution patterns of soil microfauna across ice-free coastal habitats in Victoria Land, Antarctica. Soil Biol. Biochem. 2018;116:265–276. doi: 10.1016/j.soilbio.2017.10.028. DOI

Culliney TW. Role of arthropods in maintaining soil fertility. Agriculture. 2013;3:629–659. doi: 10.3390/agriculture3040629. DOI

Krauss J, Funke W. Extraordinary high density of Protura in a windfall area of young spruce plants. Pedobiologia. 1999;43:44–46.

Malmström A, Persson T. Responses of Collembola and Protura to tree girdling - some support for ectomycorrhizal feeding. Soil Org. 2011;83:279–285.

Kubiak K, Żółciak A, Damszel M, Lech P, Sierota Z. Armillaria Pathogens under climate change. Forests. 2017;8:100. doi: 10.3390/f804010. DOI

Matějka, K. Investigation of vegetation in catchments of Plešné and Čertovo Lakes (Bohemian Forest, Czech Republic) to 2016. www.infodatasys.cz/proj002/results2016.pdf (2016).