Soil food web properties explain ecosystem services across European land use systems
Edited by William H. Schlesinger, Cary Institute of Ecosystem Studies, Millbrook, NY, and approved July 16, 2013 (received for review March 18, 2013)
Abstract
Intensive land use reduces the diversity and abundance of many soil biota, with consequences for the processes that they govern and the ecosystem services that these processes underpin. Relationships between soil biota and ecosystem processes have mostly been found in laboratory experiments and rarely are found in the field. Here, we quantified, across four countries of contrasting climatic and soil conditions in Europe, how differences in soil food web composition resulting from land use systems (intensive wheat rotation, extensive rotation, and permanent grassland) influence the functioning of soils and the ecosystem services that they deliver. Intensive wheat rotation consistently reduced the biomass of all components of the soil food web across all countries. Soil food web properties strongly and consistently predicted processes of C and N cycling across land use systems and geographic locations, and they were a better predictor of these processes than land use. Processes of carbon loss increased with soil food web properties that correlated with soil C content, such as earthworm biomass and fungal/bacterial energy channel ratio, and were greatest in permanent grassland. In contrast, processes of N cycling were explained by soil food web properties independent of land use, such as arbuscular mycorrhizal fungi and bacterial channel biomass. Our quantification of the contribution of soil organisms to processes of C and N cycling across land use systems and geographic locations shows that soil biota need to be included in C and N cycling models and highlights the need to map and conserve soil biodiversity across the world.
Acknowledgments
We thank all landowners for kindly letting us use their fields, and George Boutsis, Maria Karmezi, Sofia Nikolaou, Evangelia Boulaki, Charisis Argiropoulos, Annette Spangenberg, and Helen Quirk for help in the field and laboratory. We also thank two anonymous referees for their helpful comments on the manuscript. This project was part of the European Union Seventh Framework funded SOILSERVICE Project.
Supporting Information
Appendix (PDF)
Supporting Information
- Download
- 642.94 KB
References
1
C Stoate, et al., Ecological impacts of arable intensification in Europe. J Environ Manage 63, 337–365 (2001).
2
MB Postma-Blaauw, RGM de Goede, J Bloem, JH Faber, L Brussaard, Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91, 460–473 (2010).
3
FT de Vries, JW Van Groenigen, E Hoffland, J Bloem, Nitrogen losses from two grassland soils with different fungal biomass. Soil Biol Biochem 43, 997–1005 (2011).
4
HW Hunt, et al., The detrital food web in a shortgrass prairie. Biol Fertil Soils 3, 57–68 (1987).
5
FT de Vries, et al., Extensive management promotes plant and microbial nitrogen retention in temperate grassland. PLoS One 7, e51201 (2012).
6
J Six, SD Frey, RK Thiet, KM Batten, Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70, 555–569 (2006).
7
RD Bardgett, DA Wardle Aboveground–Belowground Linkages. Biotic Interactions, Ecosystem Processes, and Global Change (Oxford Univ Press, New York, 2010).
8
FT de Vries, RD Bardgett, Plant-microbial linkages and ecosystem N retention: Lessons for sustainable agriculture. Front Ecol Environ 10, 425–432 (2012).
9
MB Postma-Blaauw, et al., Within-trophic group interactions of bacterivorous nematode species and their effects on the bacterial community and nitrogen mineralization. Oecologia 142, 428–439 (2005).
10
H Setälä, V Huhta, Soil fauna increase Betula pendula growth: Laboratory experiments with coniferous forest floor. Ecology 72, 665–671 (1991).
11
MB Postma-Blaauw, et al., Earthworm species composition affects the soil bacterial community and net nitrogen mineralization. Pedobiologia 50, 243–256 (2006).
12
Lubbers IM, et al. (2013) Greenhouse-gas emissions from soils increased by earthworms. Nat Clim Chang 3(3):187–194.
13
S Hallin, CM Jones, M Schloter, L Philippot, Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3, 597–605 (2009).
14
SD Allison, et al., Microbial abundance and composition influence litter decomposition response to environmental change. Ecology 94, 714–725 (2013).
15
UN Nielsen, E Ayres, DH Wall, RD Bardgett, Soil biodiversity and carbon cycling: A review and synthesis of studies examining diversity-function relationships. Eur J Soil Sci 62, 105–116 (2011).
16
DH Wall, et al., Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent. Glob Chang Biol 14, 2661–2677 (2008).
17
FT de Vries, et al., Land use alters the resistance and resilience of soil food webs to drought. Nat Clim Chang 2, 276–280 (2012).
18
P Smith, Agricultural greenhouse gas mitigation potential globally, in Europe and in the UK: What have we learnt in the last 20 years? Glob Chang Biol 18, 35–43 (2012).
19
WH Schlesinger, On the fate of anthropogenic nitrogen. Proc Natl Acad Sci USA 106, 203–208 (2009).
20
D Borcard, P Legendre, All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Modell 153, 51–68 (2002).
21
FT de Vries, et al., Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities. Ecol Lett 15, 1230–1239 (2012).
22
T Helgason, TJ Daniell, R Husband, AH Fitter, JPW Young, Ploughing up the wood-wide web? Nature 394, 431 (1998).
23
FT de Vries, E Hoffland, N van Eekeren, L Brussaard, J Bloem, Fungal/bacterial ratios in grasslands with contrasting nitrogen management. Soil Biol Biochem 38, 2092–2103 (2006).
24
MN Högberg, Y Chen, P Högberg, Gross nitrogen mineralisation and fungi-to-bacteria ratios are negatively correlated in boreal forests. Biol Fertil Soils 44, 363–366 (2007).
25
D Schröter, V Wolters, PC De Ruiter, C and N mineralisation in the decomposer food webs of a European forest transect. Oikos 102, 294–308 (2003).
26
JM Fraterrigo, TC Balser, MG Turner, Microbial community variation and its relationship with nitrogen mineralization in historically altered forests. Ecology 87, 570–579 (2006).
27
W Zhang, TH Ricketts, C Kremen, K Carney, SM Swinton, Ecosystem services and dis-services to agriculture. Ecol Econ 64, 253–260 (2007).
28
MGA van der Heijden, Mycorrhizal fungi reduce nutrient loss from model grassland ecosystems. Ecology 91, 1163–1171 (2010).
29
JW Van Groenigen, GL Velthof, O Oenema, KJ Van Groenigen, C Van Kessel, Towards an agronomic assessment of N2O emissions: A case study for arable crops. Eur J Soil Sci 61, 903–913 (2010).
30
PA Niklaus, DA Wardle, KR Tate, Effects of plant species diversity and composition on nitrogen cycling and the trace gas balance of soils. Plant Soil 282, 83–98 (2006).
31
TW Willison, MS Oflaherty, P Tlustos, KWT Goulding, DS Powlson, Variations in microbial populations in soils with different methane uptake rates. Nutr Cycl Agroecosyst 49, 85–90 (1997).
32
FT de Vries, et al., Legacy effects of drought on plant growth and the soil food web. Oecologia 170, 821–833 (2012).
33
ZK Luo, et al., Meta-modeling soil organic carbon sequestration potential and its application at regional scale. Ecol Appl 23, 408–420 (2013).
34
P Ciais, S Gervois, N Vuichard, SL Piao, N Viovy, Effects of land use change and management on the European cropland carbon balance. Glob Chang Biol 17, 320–338 (2011).
35
MJ Aitkenhead, F Albanito, MB Jones, HIJ Black, Development and testing of a process-based model (MOSES) for simulating soil processes, functions and ecosystem services. Ecol Modell 222, 3795–3810 (2011).
36
NJ Ostle, et al., Integrating plant-soil interactions into global carbon cycle models. J Ecol 97, 851–863 (2009).
37
M Pulleman, et al., Soil biodiversity, biological indicators and soil ecosystem services-an overview of European approaches. Curr Opin Environ Sustain 4, 529–538 (2012).
38
C Gardi, S Jeffery, A Saltelli, An estimate of potential threats levels to soil biodiversity in EU. Glob Chang Biol 19, 1538–1548 (2013).
39
A Priemé, S Christensen, Natural perturbations, drying-wetting and freezing-thawing cycles, and the emission of nitrous oxide, carbon dioxide and methane from farmed organic soils. Soil Biol Biochem 33, 2083–2091 (2001).
40
Å Frostegård, E Bååth, The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22, 59–65 (1996).
41
PA Olsson, E Bååth, I Jakobsen, B Söderström, The use of phospholipid and neutral lipid fatty-acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol Res 99, 623–629 (1995).
42
M Klamer, E Bååth, Estimation of conversion factors for fungal biomass determination in compost using ergosterol and PLFA 18: 2 omega 6,9. Soil Biol Biochem 36, 57–65 (2004).
43
JJ S'jacob, J Van Bezooijen A Manual for Practical Work in Nematology (Wageningen University, Wageningen, The Netherlands, 1984).
Information & Authors
Information
Published in
Classifications
Submission history
Published online: August 12, 2013
Published in issue: August 27, 2013
Keywords
Acknowledgments
We thank all landowners for kindly letting us use their fields, and George Boutsis, Maria Karmezi, Sofia Nikolaou, Evangelia Boulaki, Charisis Argiropoulos, Annette Spangenberg, and Helen Quirk for help in the field and laboratory. We also thank two anonymous referees for their helpful comments on the manuscript. This project was part of the European Union Seventh Framework funded SOILSERVICE Project.
Notes
This article is a PNAS Direct Submission.
Authors
Competing Interests
The authors declare no conflict of interest.
Metrics & Citations
Metrics
Altmetrics
Citations
Cite this article
Soil food web properties explain ecosystem services across European land use systems, Proc. Natl. Acad. Sci. U.S.A.
110 (35) 14296-14301,
https://doi.org/10.1073/pnas.1305198110
(2013).
Copied!
Copying failed.
Export the article citation data by selecting a format from the list below and clicking Export.
Cited by
Loading...
View Options
View options
Download this article as a PDF file.
PDFeReader
View this article with eReader.
eReaderLogin options
Check if you have access through your login credentials or your institution to get full access on this article.
Personal login Institutional LoginRecommend to a librarian
Recommend PNAS to a LibrarianPurchase options
Purchase this article to access the full text.
