Skip to main content

Advertisement

SpringerLink
Log in

Plant species richness sustains higher trophic levels of soil nematode communities after consecutive environmental perturbations

  • Global change ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The magnitude and frequency of extreme weather events are predicted to increase in the future due to ongoing climate change. In particular, floods and droughts resulting from climate change are thought to alter the ecosystem functions and stability. However, knowledge of the effects of these weather events on soil fauna is scarce, although they are key towards functioning of terrestrial ecosystems. Plant species richness has been shown to affect the stability of ecosystem functions and food webs. Here, we used the occurrence of a natural flood in a biodiversity grassland experiment that was followed by a simulated summer drought experiment, to investigate the interactive effects of plant species richness, a natural flood, and a subsequent summer drought on nematode communities. Three and five months after the natural flooding, effects of flooding severity were still detectable in the belowground system. We found that flooding severity decreased soil nematode food-web structure (loss of K-strategists) and the abundance of plant feeding nematodes. However, high plant species richness maintained higher diversity and abundance of higher trophic levels compared to monocultures throughout the flood. The subsequent summer drought seemed to be of lower importance but reversed negative flooding effects in some cases. This probably occurred because the studied grassland system is well adapted to drought, or because drought conditions alleviated the negative impact of long-term soil waterlogging. Using soil nematodes as indicator taxa, this study suggests that high plant species richness can maintain soil food web complexity after consecutive environmental perturbations.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Blom CWPM, Voesenek LACJ (1996) Flooding: the survival strategies of plants. Trends Ecol Evol 11:290–295. doi:10.1016/0169-5347(96)10034-3

    Article  CAS  PubMed  Google Scholar 

  • Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19

    Article  PubMed  Google Scholar 

  • Bongers T (1994) De nematoden van Nederland, 2nd edn. KNNV, Utrecht

    Google Scholar 

  • Bongers T, Bongers M (1998) Functional diversity of nematodes. Appl Soil Ecol 10:239–251

    Article  Google Scholar 

  • Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14:224–228

    Article  CAS  PubMed  Google Scholar 

  • Butenschön O, Scheu S, Eisenhauer N (2011) Interactive effects of warming, soil humidity and plant diversity on litter decomposition and microbial activity. Soil Biol Biochem 43:1902–1907. doi:10.1016/j.soilbio.2011.05.011

    Article  Google Scholar 

  • Cesarz S, Reich PB, Scheu S, Ruess L, Schaefer M, Eisenhauer N (2015) Nematode functional guilds, not trophic groups, reflect shifts in soil food webs and processes in response to interacting global change factors. Pedobiologia 58:1–10. doi:10.1016/j.pedobi.2015.01.001

    Article  Google Scholar 

  • Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grünwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533. doi:10.1038/nature03972

    Article  CAS  PubMed  Google Scholar 

  • Cragg RG, Bardgett RD (2001) How changes in animal diversity within a soil trophic group influence ecosystem processes. Soil Biol Biochem 33:2073–2081. doi:10.1016/S0038-0717(01)00138-9

    Article  CAS  Google Scholar 

  • de Vries FT, Caruso T (2016) Eating from the same plate? Revisiting the role of labile carbon inputs in the soil food web. Soil Biol Biochem 102:4–9. doi:10.1016/j.soilbio.2016.06.023

    Article  PubMed  PubMed Central  Google Scholar 

  • de Vries FT, Thébault E, Liiri M, Birkhofer K, Tsiafouli MA, Bjørnlund L, Jørgensen HB, Brady MV, Christensen S, de Ruiter PC, D’Hertefeldt T, Frouz J, Hedlund K, Hemerik L, Gera Hol WH, Hotes S, Mortimer SR, Setälä H, Sgardelis SP, Uteseny K, van der Putten WH, Wolters V, Bardgett RD (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci 110:14296–14301. doi:10.1073/pnas.1305198110

    Article  PubMed  PubMed Central  Google Scholar 

  • EEA-JRC-WHO (2008) Impacts of Europe’s changing climate—2008 indicator-based assessment. EEA, Copenhagen

    Google Scholar 

  • Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB (2012) Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity. Glob Chang Biol 18:435–447. doi:10.1111/j.1365-2486.2011.02555.x

    Article  Google Scholar 

  • Evans AAF (1987) Diapause in nematodes as a survival strategy. In: Veech JA, Dickson DW (eds) Vistas on nematology. Society of Nematologists Inc, Hyattsville, pp 180–197

    Google Scholar 

  • Ferris H, Bongers T (2009) Indices developed specifically for analysis of nematode assemblages. In: Wilson MJ, Kakouli-Duarte T (eds) Nematodes as environmental indicators. CABI, Wallingford, pp 124–145

    Chapter  Google Scholar 

  • Ferris H, Bongers T, de Goede RGM (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol 18:13–29. doi:10.1016/S0929-1393(01)00152-4

    Article  Google Scholar 

  • Fischer C, Tischer J, Roscher C, Eisenhauer N (2015) Plant species diversity affects infiltration capacity in an experimental grassland through changes in soil properties. Plant Soil 397:1–16. doi:10.1007/s11104-014-2373-5

    Article  CAS  Google Scholar 

  • Fischer FM, Wright AJ, Eisenhauer N, Ebeling A, Roscher C, Wagg C, Weigelt A, Weisser WW, Pillar VD (2016) Plant species richness and functional traits affect community stability after a flood event. Philos Trans R Soc B. doi:10.1098/rstb.2015.0276

    Google Scholar 

  • Garssen AG, Baattrup-Pedersen A, Voesenek LACJ, Verhoeven JTA, Soons MB (2015) Riparian plant community responses to increased flooding: a meta-analysis. Glob Chang Biol 21:2881–2890. doi:10.1111/gcb.12921

    Article  PubMed  Google Scholar 

  • Hättenschwiler S, Gasser P (2005) Soil animals alter plant litter diversity effects on decomposition. Proc Natl Acad Sci USA 102:1519–1524. doi:10.1073/pnas.0404977102

    Article  PubMed  PubMed Central  Google Scholar 

  • Hautier Y, Seabloom EW, Borer ET, Adler PB, Harpole WS, Hillebrand H, Lind EM, MacDougall AS, Stevens CJ, Bakker JD, Buckley YM, Chu C, Collins SL, Daleo P, Damschen EI, Davies KF, Fay PA, Firn J, Gruner DS, Jin VL, Klein JA, Knops JMH, la Pierre KJ, Li W, McCulley RL, Melbourne BA, Moore JL, O’Halloran LR, Prober SM, Risch AC, Sankaran M, Schuetz M, Hector A (2014) Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508:521–525. doi:10.1038/nature13014

    Article  CAS  PubMed  Google Scholar 

  • Hines J, Eisenhauer N, Drake BG (2015) Inter-annual changes in detritus based food chains can enhance plant growth response to elevated atmospheric CO2. Glob Chang Biol 21:4642–4650. doi:10.1111/gcb.12965

    Article  PubMed  Google Scholar 

  • Hodda M, Peters L, Traunspurger W (2009) Nematode diversity in terrestrial, freshwater aquatic and marine systems. In: Wilson MJ, Kakouli-Duarte T (eds) Nematodes as Environmental Indicators. CABI, Wallingsford, pp 45–93

    Chapter  Google Scholar 

  • Hoffmann K, Bivour W, Fruh B, Koßmann M, Voß P-H (2014) Klimauntersuchungen in Jena fur die Anpassung an den Klimawandel und seine erwarteten Folgen: ein Ergebnisbericht, Berichte, d edn. Selbstverlag des Deutschen Wetterdienstes, Offenbach am Main

    Google Scholar 

  • IPCC (2013) The physical science basis. In: Contribution of Working Group I to the Fifth Assessment Report of the Intergovermental Pabel on Climate Change. Cambridge University Press, Cambridge. doi:10.1017/CBO9781107415324

  • Isbell F, Craven D, Connolly J, Loreau M, Schmid B, Beierkuhnlein C, Bezemer TM, Bonin C, Bruelheide H, de Luca E, Ebeling A, Griffin JN, Guo Q, Hautier Y, Hector A, Jentsch A, Kreyling J, Lanta V, Manning P, Meyer ST, Mori AS, Naeem S, Niklaus PA, Polley HW, Reich PB, Roscher C, Seabloom EW, Smith MD, Thakur MP, Tilman D, Tracy BF, van der Putten WH, van Ruijven J, Weigelt A, Weisser WW, Wilsey B, Eisenhauer N (2015) Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526:574–577. doi:10.1038/nature15374

    Article  CAS  PubMed  Google Scholar 

  • Jentsch A, Kreyling J, Boettcher-Treschkow J, Beierkuhnlein C (2009) Beyond gradual warming: extreme weather events alter flower phenology of European grassland and heath species. Glob Chang Biol 15:837–849. doi:10.1111/j.1365-2486.2008.01690.x

    Article  Google Scholar 

  • Jones SK, Collins SL, Blair JM, Smith MD, Knapp AK (2016) Altered rainfall patterns increase forb abundance and richness in native tallgrass prairie. Sci Rep 6:20120. doi:10.1038/srep20120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jongman B, Hochrainer-Stigler S, Feyen L, Aerts JCJH, Mechler R, Botzen WJW, Bouwer LM, Pflug G, Rojas R, Ward PJ (2014) Increasing stress on disaster-risk finance due to large floods. Nat Clim Chang 4:1–5. doi:10.1038/NCLIMATE2124

    Google Scholar 

  • Kerr RA (2007) Another global warming icon comes under attack. Science 317:28–29. doi:10.1126/science.317.5834.28a

    Article  PubMed  Google Scholar 

  • Kreyling J, Beierkuhnlein C, Elmer M, Pritsch K, Radovski M, Schloter M, Wöllecke J, Jentsch A (2008) Soil biotic processes remain remarkably stable after 100-year extreme weather events in experimental grassland and heath. Plant Soil 308:175–188. doi:10.1007/s11104-008-9617-1

    Article  CAS  Google Scholar 

  • Kröel-Dulay G, Ransijn J, Schmidt IK, Beier C, De Angelis P, de Dato G, Dukes JS, Emmett B, Estiarte M, Garadnai J, Kongstad J, Kovács-Láng E, Larsen KS, Liberati D, Ogaya R, Riis-Nielsen T, Smith AR, Sowerby A, Tietema A, Penuelas J (2015) Increased sensitivity to climate change in disturbed ecosystems. Nat Commun 6:6682. doi:10.1038/ncomms7682

    Article  PubMed  Google Scholar 

  • MacGuidwin A (1993) Management of nematodes. In: Rowe RC (ed) Potato health management. APS Press, St. Paul, MN, pp 159–166

  • Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938. doi:10.1890/11-0026.1

    Article  PubMed  Google Scholar 

  • McAleece N, Gage JDG, Lambshead PJD, Paterson GLJ (1997) BioDiversity Professional statistics analysis software. Jointly Dev. by Scottish Assoc. Mar. Sci. Nat. Hist, Museum, London

    Google Scholar 

  • Milcu A, Thebault E, Scheu S, Eisenhauer N (2010) Plant diversity enhances the reliability of belowground processes. Soil Biol Biochem 42:2102–2110. doi:10.1016/j.soilbio.2010.08.005

    Article  CAS  Google Scholar 

  • Morriën E, Hannula SE, Snoek LB, Helmsing NR, Zweers H, de Hollander M, Lu Bouffaud M, Bue M, Dimmers W, Duyts H, De Hollander M, Soto RL, Bouffaud M-L, Buée M, Dimmers W, Duyts H, Geisen S, Girlanda M, Griffiths RI, Jørgensen H-B, Jensen J, Plassart P, Redecker D, Schmelz RM, Schmidt O, Thomson BC, Tisserant E, Uroz S, Winding A, Bailey MJ, Bonkowski M, Faber JH, Martin F, Lemanceau P, de Boer W, van Veen JA, van der Putten WH (2017) Soil networks become more connected and take up more carbon as nature restoration progresses. Nat Commun 8:14349–14358. doi:10.1038/ncomms14349

    Article  PubMed  PubMed Central  Google Scholar 

  • Moyano FE, Manzoni S, Chenu C (2013) Responses of soil heterotrophic respiration to moisture availability: an exploration of processes and models. Soil Biol Biochem 59:72–85. doi:10.1016/j.soilbio.2013.01.002

    Article  CAS  Google Scholar 

  • Neher DA, Darby BJ (2009) Community indices. In: Wilson MJ, Kakouli-Duarte T (eds) Nematodes as environmental indicators. CABI, Wallingford, pp 107–123

    Chapter  Google Scholar 

  • Pérès G, Cluzeau D, Menasseri S, Soussana JF, Bessler H, Engels C, Habekost M, Gleixner G, Weigelt A, Weisser WW, Scheu S, Eisenhauer N (2013) Mechanisms linking plant community properties to soil aggregate stability in an experimental grassland plant diversity gradient. Plant Soil 373:285–299. doi:10.1007/s11104-013-1791-0

    Article  Google Scholar 

  • Pfisterer AB, Schmid B (2002) Diversity-dependent production can decrease the stability of ecosystem functioning. Nature 416:84–86. doi:10.1038/416084a

    Article  CAS  PubMed  Google Scholar 

  • Plum N (2005) Terrestrial invertebrates in flooded grassland: a literature review. Wetlands 25:721–737. doi:10.1672/0277-5212(2005)025[0721:TIIFGA]2.0.CO;2

  • Proulx R, Wirth C, Voigt W, Weigelt A, Roscher C, Attinger S, Baade J, Barnard RL, Buchmann N, Buscot F, Eisenhauer N, Fischer M, Gleixner G, Halle S, Hildebrandt A, Kowalski E, Kuu A, Lange M, Milcu A, Niklaus PA, Oelmann Y, Rosenkranz S, Sabais A, Scherber C, Scherer-Lorenzen M, Scheu S, Schulze E-D, Schumacher J, Schwichtenberg G, Soussana J-F, Temperton VM, Weisser WW, Wilcke W, Schmid B (2010) Diversity promotes temporal stability across levels of ecosystem organization in experimental grasslands. PLoS ONE 5:1–8. doi:10.1371/journal.pone.0013382

    Google Scholar 

  • Reichstein M, Bahn M, Ciais P, Frank D, Mahecha MD, Seneviratne SI, Zscheischler J, Beer C, Buchmann N, Frank DC, Papale D, Rammig A, Smith P, Thonicke K, van der Velde M, Vicca S, Walz A, Wattenbach M (2013) Climate extremes and the carbon cycle. Nature 500:287–295. doi:10.1038/nature12350

    Article  CAS  PubMed  Google Scholar 

  • Roscher C, Schumacher J, Baade J, Wilcke W, Gleixner G, Weisser WW, Schmid B, Schulze E (2004) The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community. Basic Appl Ecol 121:107–121

    Article  Google Scholar 

  • Ruess L (1995) Studies on the nematode fauna of an acid forest soil: spatial disturbance and extraction. Nematologica 41:229–239

    Article  Google Scholar 

  • Ruess L, Ferris H (2004) Decomposition pathways and successional changes. Nematol Monogr Perspect 2:547–556

    Google Scholar 

  • Scheiner SM, Gurevitch J (2001) Design and analysis of ecological experiments. Technometrics 37:432. doi:10.2307/1269183

    Google Scholar 

  • Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394. doi:10.1890/06-0219

    Article  PubMed  Google Scholar 

  • Stott P, Stone D, Allen M (2004) Changes in west Antarctic ice stream velocities: observation and analysis. Nature 432:610–614. doi:10.1029/2001JB001029

    Article  CAS  PubMed  Google Scholar 

  • Tilman D, Downing JA (1994) Biodiversity and stability in grasslands. Nature 367:363–365

    Article  Google Scholar 

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363. doi:10.1111/j.1461-0248.2008.01250.x

    Article  PubMed  Google Scholar 

  • Unger IM, Kennedy AC, Muzika R-M (2009) Flooding effects on soil microbial communities. Appl Soil Ecol 42:1–8. doi:10.1016/j.apsoil.2009.01.007

    Article  Google Scholar 

  • Visser EJW, Voesenek LA (2005) Acclimation to soil flooding-sensing and signal-transduction. Plant Soil 274:197–214. doi:10.1007/s11104-004-1650-0

    Article  CAS  Google Scholar 

  • Vogel A, Eisenhauer N, Weigelt A, Scherer-Lorenzen M (2013a) Plant diversity does not buffer drought effects on early-stage litter mass loss rates and microbial properties. Glob Chang Biol 19:2795–2803. doi:10.1111/gcb.12225

    Article  PubMed  Google Scholar 

  • Vogel A, Fester T, Eisenhauer N, Scherer-Lorenzen M, Schmid B, Weisser WW, Weigelt A (2013b) Separating drought effects from roof artifacts on ecosystem processes in a grassland drought experiment. PLoS ONE 8:e70997. doi:10.1371/journal.pone.0070997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voigt W, Perner J, Hefin Jones T (2007) Using functional groups to investigate community response to environmental changes: two grassland case studies. Glob Chang Biol 13:1710–1721. doi:10.1111/j.1365-2486.2007.01398.x

    Article  Google Scholar 

  • Wagner D, Eisenhauer N, Cesarz S (2015) Plant species richness does not attenuate responses of soil microbial and nematode communities to a flood event. Soil Biol Biochem 89:135–149. doi:10.1016/j.soilbio.2015.07.001

    Article  CAS  Google Scholar 

  • Wall DH, Bardgett RD, Kelly E (2010) Biodiversity in the dark. Nat Geosci 3:297–298. doi:10.1038/ngeo860

    Article  CAS  Google Scholar 

  • Wright AJ, Ebeling A, De Kroon H, Roscher C, Weigelt A, Buchmann N, Buchmann T, Fischer C, Hacker N, Hildebrandt A, Leimer S, Mommer L, Oelmann Y, Scheu S, Steinauer K, Strecker T, Weisser W, Wilcke W, Eisenhauer N (2015) Flooding disturbances increase resource availability and productivity but reduce stability in diverse plant communities. Nat Commun 6:1–6. doi:10.1038/ncomms7092

    Article  CAS  Google Scholar 

  • Wright AJ, De Kroon H, Visser EJW, Buchmann T, Ebeling A, Eisenhauer N, Fischer C, Hildebrandt A, Ravenek J, Roscher C, Weigelt A, Weisser W, Voesenek LACJ, Mommer L, Wright AJ (2017) Plants are less negatively affected by flooding when growing in species-rich plant communities. New Phytol 213:645–656. doi:10.1111/nph.1418

    Article  PubMed  Google Scholar 

  • Yeates GW, Bongers T, de Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologist. J. Nematol 25:315–331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yepsen RBJ (1984) The Encyclopedia of natural insect & disease control. Rodale Press, Emmaus

    Google Scholar 

Download references

Acknowledgements

The Jena Experiment is funded by the Deutsche Forschungsgemeinschaft (FOR 1451). Marcel Ciobanu gratefully acknowledges the financial support by the Transnational Access to Research Infrastructures activity in the 7th Framework Programme of the European Community under the Experimentation in Ecosystem Research (ExpeER) project for conducting the research. Further support came from the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, funded by the German Research Foundation (FZT 118). We thank Ilka Wolf, Sylvia Creutzburg and Silke Schroeckh for their help during field sampling, as well as Laura Naujoks (nematode extraction) and Daniela Wagner (nematode counting).

Author information

Authors and Affiliations

  1. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103, Leipzig, Germany

    Simone Cesarz, Alexandra J. Wright, Anja Vogel & Nico Eisenhauer

  2. Institute of Biology, Leipzig University, Deutscher Platz 5e, 04103, Leipzig, Germany

    Simone Cesarz, Anja Vogel & Nico Eisenhauer

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

    Simone Cesarz, Anne Ebeling, Anja Vogel & Nico Eisenhauer

  4. Institute of Biological Research, Branch of the National Institute of Research and Development for Biological Sciences, 48 Republicii Street, 400015, Cluj-Napoca, Romania

    Marcel Ciobanu

  5. FIT – Science & Mathematics, 227 W 27th St., New York, NY, 11201, USA

    Alexandra J. Wright

  6. Terrestrial, Ecology Research Group, School of Life Sciences Weihenstephan, Technische Universität München, Hans-Carl-von-Carlowitz-Platz 2, 85354, Freising-Weihenstephan, Germany

    Wolfgang W. Weisser

Authors
  1. Simone Cesarz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marcel Ciobanu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexandra J. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anne Ebeling
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anja Vogel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wolfgang W. Weisser
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nico Eisenhauer
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AV designed and established the drought experiment; AE, NE and WWW were responsible for the maintenance of the Jena Experiment; NE, MC and SC conceived and designed this study; MC conducted fieldwork, SC analyzed the data. SC and MC wrote the first draft of the manuscript with substantial input of AJW; all authors contributed to revisions.

Corresponding authors

Correspondence to Simone Cesarz or Marcel Ciobanu.

Additional information

Communicated by Liliane Ruess.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cesarz, S., Ciobanu, M., Wright, A.J. et al. Plant species richness sustains higher trophic levels of soil nematode communities after consecutive environmental perturbations. Oecologia 184, 715–728 (2017). https://doi.org/10.1007/s00442-017-3893-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-017-3893-5

Keywords

Search

Navigation