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Climate change and land use induce functional shifts in soil nematode communities

  • Julia SiebertEmail author
  • Marcel Ciobanu
  • Martin Schädler
  • Nico Eisenhauer
Global change ecology – original research


Land-use intensification represents one major threat to the diversity and functioning of terrestrial ecosystems. In the face of concurrent climate change, concerns are growing about the ability of intensively managed agroecosystems to ensure stable food provisioning, as they may be particularly vulnerable to climate extreme-induced harvest losses and pest outbreaks. Extensively managed systems, in contrast, were shown to mitigate climate change based on plant diversity-mediated effects, such as higher functional redundancy or asynchrony of species. In this context, the maintenance of soils is essential to sustain key ecosystem functions such as nutrient cycling, pest control, and crop yield. Within the highly diverse soil fauna, nematodes represent an important group as their trophic spectrum ranges from detritivores to predators and they allow inferences to the overall state of the ecosystem (bioindicators). Here, we investigated the effects of simulated climate change and land-use intensity on the diversity and abundance of soil nematode functional groups and functional indices in two consecutive years. We revealed that especially land use induced complex shifts in the nematode community with strong seasonal dynamics, while future climate led to weaker effects. Strikingly, the high nematode densities associated with altered climatic conditions and intensive land use were a consequence of increased densities of opportunists and potential pest species (i.e., plant feeders). This coincided with a less diverse and less structured community with presumably reduced capabilities to withstand environmental stress. These degraded soil food web conditions represent a potential threat to ecosystem functioning and underline the importance of management practices that preserve belowground organisms.


Global change Food-web complexity Food security Agroecosystem management Belowground diversity 



We thank the staff of the Bad Lauchstädt Experimental Research Station (especially Ines Merbach and Konrad Kirsch) for their work in maintaining the plots and infrastructures of the Global Change Experimental Facility (GCEF), and Harald Auge, François Buscot, and Stefan Klotz for their role in setting up the GCEF. We also thank Alla Kavtea, Claudia Breitkreuz, Tom Künne, Ulrich Pruschitzki, and Thomas Reitz for their support with lab and field work. Financial support came from the German Centre for Integrative Biodiversity Research Halle-Jena-Leipzig, funded by the German Research Foundation (FZT 118).

Author contribution statement

MS is part of the GCEF steering committee that developed the experimental platform. NE conceived the study. JS collected the data. MC identified the nematodes and calculated nematode indices. JS analyzed the data and wrote the manuscript with contributions from MC, MS, and NE.

Compliance with ethical standards

Conflict of interest

The authors declare no competing interests.

Supplementary material

442_2019_4560_MOESM1_ESM.pdf (1.1 mb)
Supplementary material 1 (PDF 1076 kb)


  1. Altermann M, Rinklebe J, Merbach I, Körschens M, Langer U, Hofmann B (2005) Chernozem—soil of the year 2005. J Plant Nutr Soil Sci 168:725–740CrossRefGoogle Scholar
  2. Bakonyi G et al (2007) Soil nematode community structure as affected by temperature and moisture in a temperate semiarid shrubland. Appl Soil Ecol 37:31–40CrossRefGoogle Scholar
  3. Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511PubMedCrossRefPubMedCentralGoogle Scholar
  4. Barnes AD et al (2018) Energy flux: the link between multitrophic biodiversity and ecosystem functioning. Trends Ecol Evol 33:186–197PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823Google Scholar
  6. Bengtsson J, Ahnström J, Weibull AC (2005) The effects of organic agriculture on biodiversity and abundance: a meta-analysis. J Appl Ecol 42:261–269Google Scholar
  7. Bernard EC (1992) Soil nematode biodiversity. Biol Fertil Soils 14:99–103CrossRefGoogle Scholar
  8. Birkhofer K et al (2011) Soil fauna feeding activity in temperate grassland soils increases with legume and grass species richness. Soil Biol Biochem 43:2200–2207CrossRefGoogle Scholar
  9. Bongers T (1988) The nematodes of the Netherlands. Stichting Uitgeverij Koninklijke Nederlandse Natuurhistorische Vereniging, Utrecht, NetherlandsGoogle Scholar
  10. Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19PubMedCrossRefPubMedCentralGoogle Scholar
  11. Bongers T, Bongers M (1998) Functional diversity of nematodes. Appl Soil Ecol 10:239–251CrossRefGoogle Scholar
  12. Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14:224–228PubMedCrossRefPubMedCentralGoogle Scholar
  13. Briones MJI, Ineson P, Piearce TG (1997) Effects of climate change on soil fauna; responses of enchytraeids, Diptera larvae and tardigrades in a transplant experiment. Appl Soil Ecol 6:117–134CrossRefGoogle Scholar
  14. Brussaard L, de Ruiter PC, Brown GG (2007) Soil biodiversity for agricultural sustainability. Agr Ecosyst Environ 121:233–244. CrossRefGoogle Scholar
  15. 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 58:23–32CrossRefGoogle Scholar
  16. Colagiero M (2011) Climate changes and nematodes: expected effects and perspectives for plant protection. Redia 94:113–118Google Scholar
  17. Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109PubMedCrossRefPubMedCentralGoogle Scholar
  18. Culman SW et al (2010) Biodiversity is associated with indicators of soil ecosystem functions over a landscape gradient of agricultural intensification. Landscape Ecol 25:1333–1348CrossRefGoogle Scholar
  19. De Long JR, Dorrepaal E, Kardol P, Nilsson M-C, Teuber LM, Wardle DA (2016) Contrasting responses of soil microbial and nematode communities to warming and plant functional group removal across a post-fire boreal forest successional gradient. Ecosystems 19:339–355CrossRefGoogle Scholar
  20. de Ruiter PC, Neutel A-M, Moore JC (1995) Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269:1257–1260PubMedPubMedCentralCrossRefGoogle Scholar
  21. De Vries FT et al (2012) Land use alters the resistance and resilience of soil food webs to drought. Nature Climate Change 2:276–280CrossRefGoogle Scholar
  22. Dendooven L, Patino-Zúniga L, Verhulst N, Luna-Guido M, Marsch R, Govaerts B (2012) Global warming potential of agricultural systems with contrasting tillage and residue management in the central highlands of Mexico. Agr Ecosyst Environ 152:50–58CrossRefGoogle Scholar
  23. Dı́az S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655CrossRefGoogle Scholar
  24. Dmowska E, Kozlowska J (1988) Communities of nematodes in soil treated with semi-liquid manure. Pedobiologia 32:323–330Google Scholar
  25. Dong Z, Hou R, Chen Q, Ouyang Z, Ge F (2013) Response of soil nematodes to elevated temperature in conventional and no-tillage cropland systems. Plant Soil 373:907–918CrossRefGoogle Scholar
  26. Doran JW, Parkin TB (1994) Defining and assessing soil quality. In: Doran JW, Coleman DC, Bezdicek BF, Stewart BA (eds) Defining soil quality for a sustainable environment. SSSA Special Publication 35, Soil Science Society of America, Madison, WI, pp 3–21Google Scholar
  27. Doscher R et al (2002) The development of the regional coupled ocean-atmosphere model RCAO. Boreal Environ Res 7:183–192Google Scholar
  28. Eisenhauer N, Migunova VD, Ackermann M, Ruess L, Scheu S (2011) Changes in plant species richness induce functional shifts in soil nematode communities in experimental grassland. PLoS One 6:e24087PubMedPubMedCentralCrossRefGoogle Scholar
  29. Evans K, Trudgill DL, Webster JM, Opperman C (1993) Plant parasitic nematodes in temperate agriculture. CAB international Wallingford, UKGoogle Scholar
  30. Ferris H (2010) Contribution of nematodes to the structure and function of the soil food web. J Nematol 42:63PubMedPubMedCentralGoogle Scholar
  31. Ferris H, Eyre M, Venette R, Lau S (1996) Population energetics of bacterial-feeding nematodes: stage-specific development and fecundity rates. Soil Biol Biochem 28:271–280CrossRefGoogle Scholar
  32. Ferris H, Bongers T, De Goede R (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol 18:13–29CrossRefGoogle Scholar
  33. Foley JA et al (2005) Global consequences of land use. Science 309:570–574PubMedCrossRefPubMedCentralGoogle Scholar
  34. Giller K, Beare M, Lavelle P, Izac A-M, Swift M (1997) Agricultural intensification, soil biodiversity and agroecosystem function. Appl Soil Ecol 6:3–16CrossRefGoogle Scholar
  35. Goldenberg SU, Nagelkerken I, Marangon E, Bonnet A, Ferreira CM, Connell SD (2018) Ecological complexity buffers the impacts of future climate on marine consumers. Nature Climate Change 8:229–233CrossRefGoogle Scholar
  36. Hautier Y et al (2014) Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508:521PubMedCrossRefPubMedCentralGoogle Scholar
  37. Hautier Y, Tilman D, Isbell F, Seabloom EW, Borer ET, Reich PB (2015) Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 348:336–340PubMedCrossRefPubMedCentralGoogle Scholar
  38. IPCC TPSB, 2007 (2007) Climate change 2007. The physical science basis. contribution of working Group I to the fourth assessment report of the intergovernmental panel on climate change [Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor and H.L. Miller (eds.)]. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USAGoogle Scholar
  39. Isbell F et al (2015) Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526:574–577PubMedCrossRefPubMedCentralGoogle Scholar
  40. Isbell F et al (2017) Benefits of increasing plant diversity in sustainable agroecosystems. J Ecol 105:871–879. CrossRefGoogle Scholar
  41. Jacob D, Podzun R (1997) Sensitivity studies with the regional climate model REMO. Meteorol Atmos Phys 63:119–129CrossRefGoogle Scholar
  42. Kardol P, Cregger MA, Campany CE, Classen AT (2010) Soil ecosystem functioning under climate change: plant species and community effects. Ecology 91:767–781PubMedCrossRefPubMedCentralGoogle Scholar
  43. Kennedy AC, Smith K (1995) Soil microbial diversity and the sustainability of agricultural soils. Plant Soil 170:75–86CrossRefGoogle Scholar
  44. Kerr RA (2007) Global Warming Is Changing the World. Science 316:188–190. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Li X et al (2019) Agriculture erases climate constraints on soil nematode communities across large spatial scales. Global Change Biol. CrossRefGoogle Scholar
  46. Lobell DB, Burke MB, Tebaldi C, Mastrandrea MD, Falcon WP, Naylor RL (2008) Prioritizing climate change adaptation needs for food security in 2030. Science 319:607–610. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Marinari S, Masciandaro G, Ceccanti B, Grego S (2000) Influence of organic and mineral fertilisers on soil biological and physical properties. Biores Technol 72:9–17CrossRefGoogle Scholar
  48. Maxwell SL, Fuller RA, Brooks TM, Watson JE (2016) Biodiversity: the ravages of guns, nets and bulldozers. Nature 536:143–145PubMedCrossRefPubMedCentralGoogle Scholar
  49. Mazancourt C et al (2013) Predicting ecosystem stability from community composition and biodiversity. Ecol Lett 16:617–625PubMedCrossRefPubMedCentralGoogle Scholar
  50. Meinke I et al (2010) Regionaler Klimaatlas Deutschland der Helmholtz-Gemeinschaft informiert im Internet über möglichen künftigen Klimawandel. Mitteilungen DMG 2:5–7Google Scholar
  51. Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr 65:21–74CrossRefGoogle Scholar
  52. Mueller KE et al (2016) Elevated CO2 and warming shift the functional composition of soil nematode communities in a semiarid grassland. Soil Biol Biochem 103:46–51CrossRefGoogle Scholar
  53. Mulder C, Zwart DD, Van Wijnen H, Schouten A, Breure A (2003) Observational and simulated evidence of ecological shifts within the soil nematode community of agroecosystems under conventional and organic farming. Funct Ecol 17:516–525CrossRefGoogle Scholar
  54. Murrell EG, Barton BT (2017) Warming alters prey density and biological control in conventional and organic agricultural systems. Integr Comp Biol 57:1–13PubMedCrossRefPubMedCentralGoogle Scholar
  55. Neher DA (2010) Ecology of plant and free-living nematodes in natural and agricultural soil. Annu Rev Phytopathol 48:371–394. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Newbold T et al (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50PubMedPubMedCentralCrossRefGoogle Scholar
  57. Nicol JM, Turner SJ, Coyne D, Den Nijs L, Hockland S, Maafi ZT (2011) Current nematode threats to world agriculture. Genomics and molecular genetics of plant-nematode interactions. Springer, Dordrecht, pp 21–43CrossRefGoogle Scholar
  58. Okada H, Harada H (2007) Effects of tillage and fertilizer on nematode communities in a Japanese soybean field. Appl Soil Ecol 35:582–598CrossRefGoogle Scholar
  59. Okada H, Harada H, Kadota I (2005) Fungal-feeding habits of six nematode isolates in the genus Filenchus. Soil Biol Biochem 37:1113–1120CrossRefGoogle Scholar
  60. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R et al. (2013) Package ‘vegan’. Community Ecology Package, Version 2.
  61. Porazinska D, Duncan L, McSorley R, Graham J (1999) Nematode communities as indicators of status and processes of a soil ecosystem influenced by agricultural management practices. Appl Soil Ecol 13:69–86CrossRefGoogle Scholar
  62. Porazinska DL et al (2003) Relationships at the aboveground–belowground interface: plants, soil biota, and soil processes. Ecol Monogr 73:377–395CrossRefGoogle Scholar
  63. Postma-Blaauw MB, de Goede RGM, Bloem J, Faber JH, Brussaard L (2010) Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91:460–473PubMedCrossRefPubMedCentralGoogle Scholar
  64. R Core Team RCT (2017) R: A language and environment for statistical computing. Vienna, Austria; 2014Google Scholar
  65. Ramirez KS, Craine JM, Fierer N (2010) Nitrogen fertilization inhibits soil microbial respiration regardless of the form of nitrogen applied. Soil Biol Biochem 42:2336–2338CrossRefGoogle Scholar
  66. Rockel B, Will A, Hense A (2008) The regional climate model COSMO-CLM (CCLM). Meteorol Z 17:347–348CrossRefGoogle Scholar
  67. Ruess L (1995) Studies on the nematode fauna of an acid forest soil: spatial distribution and extraction. Nematologica 1:229–239CrossRefGoogle Scholar
  68. Sala OE et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774PubMedPubMedCentralCrossRefGoogle Scholar
  69. Sánchez-Moreno S, Minoshima H, Ferris H, Jackson LE (2006) Linking soil properties and nematode community composition: effects of soil management on soil food webs. Nematology 8:703–715CrossRefGoogle Scholar
  70. Schädler M et al (2019) Investigating the consequences of climate change under different land-use regimes–a novel experimental infrastructure. Ecosphere. CrossRefGoogle Scholar
  71. Scialabba NE-H, Müller-Lindenlauf M (2010) Organic agriculture and climate change. Renewable Agric Food Syst 25:158–169CrossRefGoogle Scholar
  72. Siebert J, Sünnemann M, Auge H et al (2019a) The effects of drought and nutrient addition on soil organisms vary across taxonomic groups, but are constant across seasons. Sci Rep 9:639. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Siebert J et al (2019b) Extensive grassland-use sustains high levels of soil biological activity, but does not alleviate detrimental climate change effects. Adv Ecol Res 60:25CrossRefGoogle Scholar
  74. Smiley RW, Nicol JM (2009) Nematodes which challenge global wheat production. Wheat Sci Trade 10:171–187CrossRefGoogle Scholar
  75. Smith P et al (2016) Global change pressures on soils from land use and management. Glob Change Biol 22:1008–1028CrossRefGoogle Scholar
  76. Strong DR (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–754CrossRefGoogle Scholar
  77. Thakur MP et al (2014) Nematode community shifts in response to experimental warming and canopy conditions are associated with plant community changes in the temperate-boreal forest ecotone. Oecologia 175:713–723PubMedCrossRefPubMedCentralGoogle Scholar
  78. Thomas S (1978) Population densities of nematodes under seven tillage regimes. J Nematol 10:24PubMedPubMedCentralGoogle Scholar
  79. Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677CrossRefGoogle Scholar
  80. Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120PubMedCrossRefPubMedCentralGoogle Scholar
  81. Tsiafouli MA, Thébault E, Sgardelis SP, de Ruiter PC, van der Putten WH, Birkhofer K, Hemerik L, de Vries FT, Bardgett RD, Brady MV, Bjornlund L, Jørgensen HB, Christensen S, Hertefeldt TD, Hotes S, Gera Hol WH, Frouz J, Liiri M, Mortimer SR, Setälä H, Tzanopoulos J, Uteseny K, Pižl V, Stary J, Wolters V, Hedlund K (2015) Intensive agriculture reduces soil biodiversity across Europe. Glob Change Biol 21(2):973–985PubMedCrossRefPubMedCentralGoogle Scholar
  82. Voigt W, Perner J, Hefin Jones T (2007) Using functional groups to investigate community response to environmental changes: two grassland case studies. Glob Change Biol 13:1710–1721CrossRefGoogle Scholar
  83. 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 89:135–149CrossRefGoogle Scholar
  84. Wall DH, Nielsen UN, Six J (2015) Soil biodiversity and human health. Nature 528(7580):69–76PubMedCrossRefPubMedCentralGoogle Scholar
  85. Wardle D, Yeates G, Watson R, Nicholson K (1995) The detritus food-web and the diversity of soil fauna as indicators of disturbance regimes in agro-ecosystems. Plant Soil 170:35–43CrossRefGoogle Scholar
  86. Wasilewska L (1997) Soil invertebrates as bioindicators, with special reference to soil-inhabiting nematodes. Russian J Nematol 5:113–126Google Scholar
  87. Wheeler T, Von Braun J (2013) Climate change impacts on global food security. Science 341:508–513PubMedCrossRefPubMedCentralGoogle Scholar
  88. Whitehead AG (1997) Plant nematode control. CAB International, Wallingford (UK)Google Scholar
  89. Wilby A, Thomas MB (2002) Natural enemy diversity and pest control: patterns of pest emergence with agricultural intensification. Ecol Lett 5:353–360CrossRefGoogle Scholar
  90. Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci 96:1463–1468. CrossRefPubMedPubMedCentralGoogle Scholar
  91. Yagioka A, Komatsuzaki M, Kaneko N, Ueno H (2015) Effect of no-tillage with weed cover mulching versus conventional tillage on global warming potential and nitrate leaching. Agr Ecosyst Environ 200:42–53CrossRefGoogle Scholar
  92. Yan X, Wang K, Song L, Wang X, Wu D (2017) Daytime warming has stronger negative effects on soil nematodes than night-time warming. Sci Rep 7:44888PubMedPubMedCentralCrossRefGoogle Scholar
  93. Yeates G, Bird A (1994) Some observations on the influence of agricultural practices on the nematode faunae of some South Australian soils. Fundam Appl Nematol 17:133–145Google Scholar
  94. Yeates G, Wardle D (1996) Nematodes as predators and prey: relationships to biological control and soil processes. Pedobiologia 40:43–50Google Scholar
  95. Yeates G, Bongers T, De Goede R, Freckman D, Georgieva S (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25:315PubMedPubMedCentralGoogle Scholar
  96. Yeates G, Wardle D, Watson R (1999) Responses of soil nematode populations, community structure, diversity and temporal variability to agricultural intensification over a seven-year period. Soil Biol Biochem 31:1721–1733CrossRefGoogle Scholar
  97. Yeates G, Dando J, Shepherd T (2002) Pressure plate studies to determine how moisture affects access of bacterial-feeding nematodes to food in soil. Eur J Soil Sci 53:355–365CrossRefGoogle Scholar
  98. Zhang X, Li Q, Zhu A, Liang W, Zhang J, Steinberger Y (2012) Effects of tillage and residue management on soil nematode communities in North China. Ecol Ind 13:75–81CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany
  2. 2.Institute of Biology, Leipzig UniversityLeipzigGermany
  3. 3.Institute of Biological Research, Branch of the National Institute of Research and Development for Biological SciencesCluj-NapocaRomania
  4. 4.Department of Community EcologyHelmholtz-Centre for Environmental Research – UFZHalleGermany

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