Skip to main content
Log in

Roots rather than shoot residues drive soil arthropod communities of arable fields

  • Plant-microbe-animal interactions - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Soil food webs are driven by plant-derived carbon (C) entering the soil belowground as rhizodeposits or aboveground via leaf litter, with recent research pointing to a higher importance of the former for driving forest soil food webs. Using natural abundance stable isotopes of wheat (C3 plant) and maize (C4 plant), we followed and quantified the incorporation of shoot residue- and root-derived maize C into the soil animal food web of an arable field for 1 year, thereby disentangling the importance of shoot residue- versus root-derived resources for arable soil food webs. On average, shoot residue-derived resources only contributed less than 12 % to soil arthropod body C, while incorporation of root-derived resources averaged 26 % after 2 months of maize crop and increased to 32 % after 1 year. However, incorporation of root-derived maize C did not consistently increase with time: rather, it increased, decreased or remained constant depending on species. Further, preference of shoot residue- or root-derived resources was also species-specific with about half the species incorporating mainly root-derived C, while only a few species preferentially incorporated shoot residue-derived C, and about 40 % incorporated both shoot residue- as well as root-derived C. The results highlight the predominant importance of root-derived resources for arable soil food webs and suggest that shoot residues only form an additional resource of minor importance. Variation in the use of plant-derived C between soil arthropod species suggests that the flux of C through soil food webs of arable systems can only be disentangled by adopting a species-specific approach.

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

Access this article

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

  • Albers D, Schaefer M, Scheu S (2006) Incorporation of plant carbon into the soil animal food web of an arable system. Ecology 87:235–245. doi:10.1890/04-1728

    Article  PubMed  Google Scholar 

  • Andresen LC, Konestabo HS, Maraldo K, Holmstrup M, Ambus P, Beier C, Michelsen A (2011) Organic matter flow in the food web at a temperate heath under multifactorial climate change. Rap Comm Mass Sp 25:1485–1496. doi:10.1002/rcm.4907

    Article  CAS  Google Scholar 

  • Arrouays D, Balesdent J, Mariotti A, Girardin C (1995) Modeling organic-carbon turnover in cleared temperate forest soils converted to maize cropping by using C-13 natural-abundance measurements. Plant Soil 173:191–196. doi:10.1007/bf00011455

    Article  CAS  Google Scholar 

  • Bardgett RD (2005) The biology of soil: a community and ecosystem approach, 1st edn. Oxford University Press, Oxford

  • Berg MP, Stoffer M, van den Heuvel HH (2004) Feeding guilds in Collembola based on digestive enzymes. Pedobiologia 48:589–601. doi:10.1016/j.pedobi.2004.07.006

    Article  Google Scholar 

  • Bradford MA, Strickland MS, DeVore JL, Maerz JC (2012) Root carbon flow from an invasive plant to belowground foodwebs. Plant Soil 359:233–244. doi:10.1007/s11104-012-1210-y

    Article  CAS  Google Scholar 

  • Briones MJI, Garnett MH, Piearce TG (2005) Earthworm ecological groupings based on 14C analysis. Soil Biol Biochem 37:2145–2149. doi:10.1016/j.soilbio.2005.03.001

    Article  CAS  Google Scholar 

  • Buryn R, Brandl R (1992) Are the morphometrics of chelicerae correlated with diet in mesostigmatid mites (Acari)? Exp Appl Acarol 14:67–82. doi:10.1007/BF01205353

    Article  Google Scholar 

  • Buse T, Ruess L, Filser J (2013) New trophic biomarkers for Collembola reared on algal diets. Pedobiologia 56:153–159. doi:10.1016/j.pedobi.2013.03.005

    Article  Google Scholar 

  • Caner L, Zeller B, Dambrine É, Ponge J-F, Chauvat M, Llanque C (2004) Origin of the nitrogen assimilated by soil fauna living in decomposing beech litter. Soil Biol Biochem 36:1861–1872. doi:10.1016/j.soilbio.2004.05.007

    Article  CAS  Google Scholar 

  • Cebrian J, Lartigue J (2004) Patterns of herbivory and decomposition in aquatic and terrestrial ecosystems. Ecol Monogr 74:237–259. doi:10.1890/03-4019

    Article  Google Scholar 

  • Chahartaghi M, Langel R, Scheu S, Ruess L (2005) Feeding guilds in Collembola based on nitrogen stable isotope ratios. Soil Biol Biochem 37:1718–1725. doi:10.1016/j.soilbio.2005.02.006

    Article  CAS  Google Scholar 

  • Crowther TW, Boddy L, Jones TH (2011) Species-specific effects of soil fauna on fungal foraging and decomposition. Oecologia 167:535–545. doi:10.1007/s00442-011-2005-1

    Article  PubMed  Google Scholar 

  • Dennis P, Wratten SD, Sotherton NW (1991) Mycophagy as a factor limiting predation of aphids (Hemiptera: Aphididae) by staphylinid beetles (Coleoptera: Staphylinidae) in cereals. Bull Entomol Res 81:25–31. doi:10.1017/S0007485300053207

    Article  Google Scholar 

  • Digel C, Curtsdotter A, Riede J, Klarner B, Brose U (2014) Unravelling the complex structure of forest soil food webs: higher omnivory and more trophic levels. Oikos 123:1157–1172. doi:10.1111/oik.00865

    Article  Google Scholar 

  • Eissfeller V, Beyer F, Valtanen K, Hertel D, Maraun M, Polle A, Scheu S (2013) Incorporation of plant carbon and microbial nitrogen into the rhizosphere food web of beech and ash. Soil Biol Biochem 62:76–81. doi:10.1016/j.soilbio.2013.03.002

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fox J (2003) Effect displays in R for generalised linear models. J Stat Softw 8:1–27

    Article  Google Scholar 

  • Frouz J (1999) Use of soil dwelling Diptera (Insecta, Diptera) as bioindicators: a review of ecological requirements and response to disturbance. Agric Ecosyst Environ 74:167–186. doi:10.1016/S0167-8809(99)00036-5

    Article  Google Scholar 

  • Gunn A, Cherrett JM (1993) The exploitation of food resources by soil meso- and macrofauna invertebrates. Pedobiologia 37:303–320

    Google Scholar 

  • Haubert D, Birkhofer K, Fließbach A, Gehre M, Scheu S, Ruess L (2009) Trophic structure and major trophic links in conventional versus organic farming systems as indicated by carbon stable isotope ratios of fatty acids. Oikos 118:1579–1589. doi:10.1111/j.1600-0706.2009.17587.x

    Article  CAS  Google Scholar 

  • Heidemann K, Hennies A, Schakowske J, Blumenberg L, Ruess L, Scheu S, Maraun M (2014) Free-living nematodes as prey for higher trophic levels of forest soil food webs. Oikos 123:1199–1211. doi:10.1111/j.1600-0706.2013.00872.x

    Article  CAS  Google Scholar 

  • Hopkin SP (2007) A Key to the Collembola (Springtails) of Britain and Ireland, 1st edn. Field Studies Council, London

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363. doi:10.1002/bimj.200810425

    Article  Google Scholar 

  • Karg W (1993) Die Tierwelt Deutschlands 59-Raubmilben, 2nd edn. Gustav Fischer, Jena

  • Kempson D, Lloyd M, Ghelardi M (1963) A new extractor for woodland litter. Pedobiologia 3:1–21

    Google Scholar 

  • Klarner B, Maraun M, Scheu S (2013) Trophic diversity and niche partitioning in a species rich predator guild—Natural variations in stable isotope ratios (13C/12C, 15N/14N) of mesostigmatid mites (Acari, Mesostigmata) from Central European beech forests. Soil Biol Biochem 57:327–333. doi:10.1016/j.soilbio.2012.08.013

    Article  CAS  Google Scholar 

  • Koehler HH (1997) Mesostigmata (Gamasina, Uropodina), efficient predators in agroecosystems. Agric Ecosyst Environ 62:105–117. doi:10.1016/S0167-8809(96)01141-3

    Article  Google Scholar 

  • Kramer S, Marhan S, Ruess L, Armbruster W, Butenschoen O, Haslwimmer H, Kuzyakov Y, Pausch J, Scheunemann N, Schoene J, Schmalwasser A, Totsche KU, Walker F, Scheu S, Kandeler E (2012) Carbon flow into microbial and fungal biomass as a basis for the belowground food web of agroecosystems. Pedobiologia 55:111–119. doi:10.1016/j.pedobi.2011.12.001

    Article  CAS  Google Scholar 

  • Kramer S, Marhan S, Haslwimmer H, Ruess L, Kandeler E (2013) Temporal variation in surface and subsoil abundance and function of the soil microbial community in an arable soil. Soil Biol Biochem 61:76–85. doi:10.1016/j.soilbio.2013.02.006

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review. J Plant Nutr Soil Sci 163:421–431. doi:10.1002/1522-2624(200008)163:4<421::AID-JPLN421>3.0.CO;2-R

    Article  CAS  Google Scholar 

  • Lal R (2004a) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627. doi:10.1126/science.1097396

    Article  CAS  PubMed  Google Scholar 

  • Lal R (2004b) Soil carbon sequestration to mitigate climate change. Geoderma 123:1–22. doi:10.1016/j.geoderma.2004.01.032

    Article  CAS  Google Scholar 

  • Langel R, Dyckmans J (2014) Combined 13C and 15N isotope analysis on small samples using a near-conventional elemental analyzer/isotope ratio mass spectrometer setup. Rap Comm Mass Sp 28:1019–1022. doi:10.1002/rcm.6878

    Article  CAS  Google Scholar 

  • Leake JR, Ostle NJ, Rangel-Castro JI, Johnson D (2006) Carbon fluxes from plants through soil organisms determined by field 13CO2 pulse-labelling in an upland grassland. Appl Soil Ecol 33:152–175. doi:10.1016/j.apsoil.2006.03.001

    Article  Google Scholar 

  • Lehman RM, Osborne SL, Rosentrater KA (2008) No differences in decomposition rates observed between Bacillus thuringiensis and non-Bacillus thuringiensis corn residue incubated in the field. Agron J 100:163–168. doi:10.2134/agronj2007.0123

    Article  Google Scholar 

  • Martin A, Balesdent J, Mariotti A (1992) Earthworm diet related to soil organic matter dynamics through 13C measurements. Oecologia 91:23–29. doi:10.1007/BF00317236

    Article  Google Scholar 

  • Moore JC, Berlow EL, Coleman DC, de Ruiter PC, Dong Q, Hastings A, Collins Johnson N, McCann KS, Melville K, Morin PJ, Nadelhoffer K, Rosemond AD, Post DM, Sabo JL, Scow KM, Vanni MJ, Wall DH (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600. doi:10.1111/j.1461-0248.2004.00606.x

    Article  Google Scholar 

  • Nielsen LB, Nielsen BO (2002) Density and phenology of soil gallmidges (Diptera: Cecidomyiidae) in arable land. Pedobiologia 46:1–14. doi:10.1078/0031-4056-00108

    Article  Google Scholar 

  • Noordijk J, Musters CJM, Dijk J, Snoo GR (2010) Invertebrates in field margins: taxonomic group diversity and functional group abundance in relation to age. Biodivers Conserv 19:3255–3268. doi:10.1007/s10531-010-9890-1

    Article  Google Scholar 

  • Pausch J, Kuzyakov Y (2012) Soil organic carbon decomposition from recently added and older sources estimated by δ13C values of CO2 and organic matter. Soil Biol Biochem 55:40–47. doi:10.1016/j.soilbio.2012.06.007

    Article  CAS  Google Scholar 

  • Pausch J, Kramer S, Scharroba A, Scheunemann N, Butenschoen O, Kandeler E, Marhan S, Riederer M, Scheu S, Kuzyakov Y, Ruess L (2015) Small but active – pool size does not matter for carbon incorporation in below-ground food webs. Functional Ecology. doi:10.1111/1365-2435.12512

    Google Scholar 

  • Perdomo G, Evans A, Maraun M, Sunnucks P, Thompson R (2012) Mouthpart morphology and trophic position of microarthropods from soils and mosses are strongly correlated. Soil Biol Biochem 53:56–63. doi:10.1016/j.soilbio.2012.05.002

    Article  CAS  Google Scholar 

  • Petersen BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Evol S 18:293–320

    Article  Google Scholar 

  • Pfiffner L, Luka H (2000) Overwintering of arthropods in soils of arable fields and adjacent semi-natural habitats. Agric Ecosyst Environ 78:215–222. doi:10.1016/S0167-8809(99)00130-9

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, The R Development Team (2013) NLME: linear and nonlinear mixed effects models. R package version 3.1-111

  • Pollierer MM, Langel R, Körner C, Maraun M, Scheu S (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736. doi:10.1111/j.1461-0248.2007.01064.x

    Article  PubMed  Google Scholar 

  • Pollierer MM, Dyckmans J, Scheu S, Haubert D (2012) Carbon flux through fungi and bacteria into the forest soil animal food web as indicated by compound-specific 13C fatty acid analysis. Funct Ecol 26:978–990. doi:10.1111/j.1365-2435.2012.02005.x

    Article  Google Scholar 

  • Ponsard S, Arditi R (2000) What can stable isotopes (d15N and d13C) tell about the food web of soil macro-invertebrates? Ecology 81:852–864. doi:10.1890/0012-9658(2000)081

    Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83:703–718. doi:10.1890/0012-9658(2002)083

    Article  Google Scholar 

  • 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 91:460–473. doi:10.1890/09-0666.1

    Article  PubMed  Google Scholar 

  • R Core Team T (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B:81–99. doi:10.1034/j.1600-0889.1992.t01-1-00001.x

    Article  CAS  Google Scholar 

  • Read DS, Sheppard SK, Bruford MW, Glen M, Symondson WOC (2006) Molecular detection of predation by soil micro-arthropods on nematodes. Mol Ecol 15:1963–1972. doi:10.1111/j.1365-294X.2006.02901.x

    Article  CAS  PubMed  Google Scholar 

  • Reineking A, Langel R, Schikowski J (1993) 15N, 13C-on-line measurements with an elemental analyser (Carlo Erba, NA 1500), a modified trapping box and a gas isotope mass spectrometer (FINNIGAN, MAT 251). Isotopenpraxis Environ Health Stud 29:169–174. doi:10.1080/10256019308046151

    Article  CAS  Google Scholar 

  • Schaefer M (2010) Brohmer-Fauna von Deutschland, 23rd edn. Quelle and Meyer, Wiebelsheim

  • Scharroba A, Dibbern D, Hünninghaus M, Kramer S, Moll J, Butenschoen O, Bonkowski M, Buscot F, Kandeler E, Koller R, Krüger D, Lueders T, Scheu S, Ruess L (2012) Effects of resource availability and quality on the structure of the micro-food web of an arable soil across depth. Soil Biol Biochem 50:1–11. doi:10.1016/j.soilbio.2012.03.002

    Article  CAS  Google Scholar 

  • Scheu S, Setälä H (2002) Multitrophic interactions in decomposer food webs. In: Hawkins BA, Tscharntke T (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 223–264

  • Scheunemann N, Scheu S, Butenschoen O (2010) Incorporation of decade old soil carbon into the soil animal food web of an arable system. Appl Soil Ecol 46:59–63. doi:10.1016/j.apsoil.2010.06.014

    Article  Google Scholar 

  • Scheunemann N, Maraun M, Scheu S, Butenschoen O (2015) The role of shoot residues vs. crop species for soil arthropod diversity and abundance of arable systems. Soil Biol Biochem 81:81–88. doi:10.1016/j.soilbio.2014.11.006

    Article  CAS  Google Scholar 

  • Schneider K, Maraun M (2005) Feeding preferences among dark pigmented fungal taxa (“Dematiacea”) indicate limited trophic niche differentiation of oribatid mites (Oribatida, Acari). Pedobiologia 49:61–67. doi:10.1016/j.pedobi.2004.07.010

    Article  Google Scholar 

  • Schneider K, Migge-Kleian S, Norton RA, Scheu S, Langel R, Reineking A, Maraun M (2004) Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15N/14N). Soil Biol Biochem 36:1769–1774. doi:10.1016/j.soilbio.2004.04.033

    Article  CAS  Google Scholar 

  • Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Richter A, Eberl L, Zechmeister-Boltenstern S, Riedel K (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 6:1749–1762. doi:10.1038/ismej.2012.11

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Semenyuk II, Tiunov AV (2011) Isotopic signature (15N/14N and 13C/12C) confirms similarity of trophic niches of millipedes (Myriapoda, Diplopoda) in a temperate deciduous forest. Biol Bull 38:283–291. doi:10.1134/S1062359011030137

    Article  CAS  Google Scholar 

  • Spain AV, Saffigna PG, Wood AW (1990) Tissue carbon sources for Pontoscolex corethrurus (Oligochaeta: Glossoscolecidae) in a sugarcane ecosystem. Soil Biol Biochem 22:703–706. doi:10.1016/0038-0717(90)90018-U

    Article  CAS  Google Scholar 

  • von Berg K, Thies C, Tscharntke T, Scheu S (2010) Changes in herbivore control in arable fields by detrital subsidies depend on predator species and vary in space. Oecologia 163:1033–1042. doi:10.1007/s00442-010-1604-6

    Article  Google Scholar 

  • Vreeken-Buijs MJ, Geurs M, De Ruiter PC, Brussaard L (1994) Microarthropod biomass-C dynamics in the belowground food webs of two arable farming systems. Agric Ecosyst Environ 51:161–170. doi:10.1016/0167-8809(94)90041-8

    Article  Google Scholar 

  • Wang X, Sun B, Mao J, Sui Y, Cao X (2012) Structural convergence of maize and wheat straw during two-year decomposition under different climate conditions. Environ Sci Technol 46:7159–7165. doi:10.1021/es300522x

    Article  CAS  PubMed  Google Scholar 

  • Weigmann G (2006) Die Tierwelt Deutschlands Teil 76—Hornmilben (Oribatida), 1st edn. Goecke and Evers, Keltern

  • Wolkovich EM, Allesina S, Cottingham KL, Moore JC, Sandin SA, de Mazancourt C (2014) Linking the green and brown worlds: the prevalence and effect of multi-channel feeding in food webs. Ecology 95:3376–3386. doi:10.1890/13-1721.1

    Article  Google Scholar 

Download references

Acknowledgments

We thank Reinhard Langel (Kompetenzzentrum Stabile Isotope, University of Göttingen) for analysis of stable isotopes. Thanks to Bernhard Klarner and Verena Eißfeller for help in identifying Gamasida and Oribatida, respectively, and to Sarah Zieger for advice in using R. Many students helped in taking samples in the field, harvesting maize and adding maize residues. Financial support was provided by the German Research Foundation (DFG) within the Research Unit “Carbon flow in belowground food webs assessed by isotope tracers” (FOR 918).

Author contribution statement

SS and OB designed the experiment. NS and OB conducted fieldwork. NS identified species and prepared stable isotope analyses. NS and CD performed statistical analyses. NS, OB and SS wrote the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicole Scheunemann.

Additional information

Communicated by Evan Siemann.

S. Scheu and O. Butenschoen contributed equally.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 27 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Scheunemann, N., Digel, C., Scheu, S. et al. Roots rather than shoot residues drive soil arthropod communities of arable fields. Oecologia 179, 1135–1145 (2015). https://doi.org/10.1007/s00442-015-3415-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3415-2

Keywords

Navigation