Abstract
Climate warming is predicted to alter the structure, stability, and functioning of food webs1,2,3,4,5. Yet, despite the importance of soil food webs for energy and nutrient turnover in terrestrial ecosystems, the effects of warming on these food webs—particularly in combination with other global change drivers—are largely unknown. Here, we present results from two complementary field experiments that test the interactive effects of warming with forest canopy disturbance and drought on energy flux in boreal–temperate ecotonal forest soil food webs. The first experiment applied a simultaneous above- and belowground warming treatment (ambient, +1.7 °C, +3.4 °C) to closed-canopy and recently clear-cut forest, simulating common forest disturbance6. The second experiment crossed warming with a summer drought treatment (−40% rainfall) in the clear-cut habitats. We show that warming reduces energy flux to microbes, while forest canopy disturbance and drought facilitates warming-induced increases in energy flux to higher trophic levels and exacerbates the reduction in energy flux to microbes, respectively. Contrary to expectations, we find no change in whole-network resilience to perturbations, but significant losses in ecosystem functioning. Warming thus interacts with forest disturbance and drought, shaping the energetic structure of soil food webs and threatening the provisioning of multiple ecosystem functions in boreal–temperate ecotonal forests.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Yvon-Durocher, G., Montoya, J. M., Trimmer, M. & Woodward, G. Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems. Glob. Change Biol. 17, 1681–1694 (2011).
Petchey, O. L., McPhearson, P. T., Casey, T. M. & Morin, P. J. Environmental warming alters food-web structure and ecosystem function. Nature 402, 69–72 (1999).
Binzer, A., Guill, C., Rall, B. C. & Brose, U. Interactive effects of warming, eutrophication and size structure: Impacts on biodiversity and food-web structure. Glob. Change Biol. 22, 220–227 (2016).
O’Connor, M. I., Piehler, M. F., Leech, D. M., Anton, A. & Bruno, J. F. Warming and resource availability shift food web structure and metabolism. PLoS Biol. 7, 3–8 (2009).
Woodward, G. et al. Ecological networks in a changing climate. Adv. Ecol. Res. 42, 72–138 (2010).
Rich, R. L. et al. Design and performance of combined infrared canopy and belowground warming in the B4WarmED (Boreal Forest Warming at an Ecotone in Danger) experiment. Glob. Change Biol. 21, 2105–2464 (2015).
Fussmann, K. E., Schwarzmüller, F., Brose, U., Jousset, A. & Rall, B. C. Ecological stability in response to warming. Nat. Clim. Change 4, 206–210 (2014).
Thakur, M. P., Künne, T., Griffin, J. N. & Eisenhauer, N. Warming magnifies predation and reduces prey coexistence in a model litter arthropod system. Proc. R. Soc. B 284, 20162570 (2017).
Rip, J. M. K. & McCann, K. S. Cross-ecosystem differences in stability and the principle of energy flux. Ecol. Lett. 14, 733–740 (2011).
de Ruiter, P. C., Neutel, A.-M. M. & Moore, J. C. Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269, 1257–1260 (1995).
Gilbert, B. et al. A bioenergetic framework for the temperature dependence of trophic interactions. Ecol. Lett. 17, 902–914 (2014).
Barnes, A. D. et al. Consequences of tropical land use for multitrophic biodiversity and ecosystem functioning. Nat. Commun. 5, 5351 (2014).
Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. B. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).
Ehnes, R. B., Rall, B. C. & Brose, U. Phylogenetic grouping, curvature and metabolic scaling in terrestrial invertebrates. Ecol. Lett. 14, 993–1000 (2011).
Rall, B. C., Vucic-Pestic, O., Ehnes, R. B., Emmerson, M. & Brose, U. Temperature, predator-prey interaction strength and population stability. Glob. Change. Biol. 16, 2145–2157 (2010).
De Vries, F. et al. Land use alters the resistance and resilience of soil food webs to drought. Nat. Clim. Change. 2, 276–280 (2012).
Ledger, M. E., Brown, L. E., Edwards, F. K., Milner, A. M. & Woodward, G. Drought alters the structure and functioning of complex food webs. Nat. Clim. Change. 3, 223–227 (2012).
Cebrian, J. Patterns in the fate of production in plant communities. Am. Nat. 154, 449–468 (1999).
Wall, D. H., Nielsen, U. N. & Six, J. Soil biodiversity and human health. Nature 528, 69–76 (2015).
De Ruiter, P. C. De et al. Simulation of nitrogen mineralization in the below-ground food webs of two winter wheat fields. J. Appl. Ecol. 30, 95–106 (1993).
Bradford, M. A. et al. Managing uncertainty in soil carbon feedbacks to climate change. Nat. Clim. Change. 6, 751–758 (2016).
Lang, B., Rall, B. C., Scheu, S. & Brose, U. Effects of environmental warming and drought on size-structured soil food webs. Oikos 123, 1224–1233 (2014).
DeAngelis, K. M. et al. Long-term forest soil warming alters microbial communities in temperate forest soils. Front. Microbiol. 6, 1–13 (2015).
Kardol, P., Reynolds, W. N., Norby, R. J. & Classen, A. T. A. T. Climate change effects on soil microarthropod abundance and community structure. Appl. Soil Ecol. 47, 37–44 (2011).
Thakur, M. P. et al. 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, 713–723 (2014).
Bradford, M. A. et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11, 1316–1327 (2008).
Hunt, H. W. et al. The detrital food web in a shortgrass prairie. Biol. Fertil. Soils 3, 57–68 (1987).
Adu, J. K. & Oades, J. M. Utilization of organic materials in soil aggregates by bacteria and fungi. Soil Biol. Biochem. 10, 117–122 (1978).
Eisenhauer, N. et al. Organic textile dye improves the visual assessment of the bait-lamina test. Appl. Soil Ecol. 82, 78–81 (2014).
Neutel, A. M. et al. Reconciling complexity with stability in naturally assembling food webs. Nature 449, 599–602 (2007).
Thakur, M. P. et al. Effects of soil warming history on the performances of congeneric temperate and boreal herbaceous plant species and their associations with soil biota. J. Plant Ecol. 10, 670–680 (2017).
Scheu, S. Automated measurement of the respiratory response of soil microcompartments: active microbial biomass in earthworm faeces. Soil Biol. Biochem. 24, 1–6 (1992).
Anderson, J. & Domsch, K. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol. Biochem. 10, 215–221 (1978).
Beck, T. et al. An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biol. Biochem. 29, 1023–1032 (1997).
Ruess, L. Studies on the nematode fauna of an acid forest soil: spatial distribution and extraction. Nematologica 41, 229–239 (1995).
Bongers, T. De nematoden van Nederland; een Identificatietabel voor de in Nederland Aangetroffen Zoetwater-en Bodembewonende Nematoden (KNNV Uitgeverij, Utrecht, 1988).
Yeates, G. W., Bongers, T., De Goede, R. G., Freckman, D. W. & Georgieva, S. S. Feeding habits in soil nematode families and genera-an outline for soil ecologists. J. Nematol. 25, 315–331 (1993).
Okada, H., Harada, H. & Kadota, I. Fungal-feeding habits of six nematode isolates in the genus Filenchus. Soil Biol. Biochem. 37, 1113–1120 (2005).
Yeates, G. W. Soil nematodes in terrestrial ecosystems. J. Nematol. 11, 213–229 (1979).
Holtkamp, R. et al. Soil food web structure during ecosystem development after land abandonment. Appl. Soil Ecol. 39, 23–34 (2008).
Kempson, D., Lloyd, M. & Ghelardi, R. A new extractor for woodland litter. Pedobiologia 3, 1–21 (1963).
Schäfer, M. & Brohmer, P. Fauna von Deutschland: ein Bestimmungsbuch unserer heimischen Tierwelt (Quelle & Meyer, Wiebelsheim, 2006).
Crotty, F. & Shepherd, M. A Key to Soil Mites in the UK (Field Studies Council, 2014); http://tombio.myspecies.info/files/MitesKeyTest-2014-03-07.pdf
Swift, M. J., Heal, O. W. & Anderson, J. M. Decomposition in Terrestrial Ecosystems 5 (Univ. California Press, Berkeley and Los Angeles, 1979).
Edwards, C. A. in Progress in Soil Biology (eds Graff, O. & Satchell, J.) 585–591 (North-Holland Publishing Company, New York, 1967).
Mercer, R. D., Gabriel, A. G. A., Barendse, J., Marshall, D. J. & Chown, S. L. Invertebrate body sizes from Marion Island. Antarct. Sci. 13, 135–143 (2001).
Teuben, A. & Verhoef, H. A. Direct contribution by soil arthropods to nutrient availability through body and faecal nutrient content. Biol. Fertil. Soils 14, 71–75 (1992).
Berg, M. et al. Community food web, decomposition and nitrogen mineralisation in a stratified Scots pine forest soil. Oikos 94, 130–142 (2001).
Didden, W. A. M. et al. Soil meso- and macrofauna in two agricultural systems: factors affecting population dynamics and evaluation of their role in carbon and nitrogen dynamics. Agric. Ecosyst. Environ. 51, 171–186 (1994).
Freckman, D. W. & Caswell, E. P. The ecology of nematodes in agroecosystems. Annu. Rev. Phytopathol. 23, 275–296 (1985).
Petersen, H. & Luxton, M. A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39, 288 (1982).
Pollierer, M. M., Langel, R., Scheu, S. & Maraun, M. Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15N/14N and 13C/12C). Soil Biol. Biochem. 41, 1221–1226 (2009).
Walter, D. E. & Proctor, H. C. Mites: Ecology, Evolution and Behaviour (Springer, Dordrecht Heidelberg, New York, London, 1999).
Andrén, O. et al. Organic carbon and nitrogen flows. Ecol. Bull. 40, 85–126 (1990).
Walter, D. E. & Ikonen, E. K. Species, guilds, and functional groups: taxonomy and behavior in nematophagous arthropods. J. Nematol. 21, 315–327 (1989).
Scheu, S. & Falca, M. The soil food web of two beech forests (Fagus sylvatica) of contrasting humus type: stable isotope analysis of a macro- and a mesofauna-dominated community. Oecologia 123, 285–296 (2000).
Peters, R. H. The Ecological Implications of Body Size (Cambridge University Press, Cambridge, 1983).
Wardle, D. A. & Ghani, A. A critique of the microbial metabolic quotient (qCO2) as a bioindicator of disturbance and ecosystem development. Soil Biol. Biochem. 27, 1601–1610 (1995).
Salonen, K., Sarvala, J., Hakala, I. & Viljanen, M. L. Relation of energy and organic-carbon in aquatic invertebrates. Limnol. Oceanogr. 21, 724–730 (1976).
Gongalsky, K. B., Persson, T. & Pokarzhevskii, A. D. Effects of soil temperature and moisture on the feeding activity of soil animals as determined by the bait-lamina test. Appl. Soil Ecol. 39, 84–90 (2008).
von Törne, E. Assessing feeding activities of soil-living animals. I. Bait-lamina-tests. Pedobiologia 34, 89–101 (1990).
Neutel, A.-M., Heesterbeek, J. A. P. & de Ruiter, P. C. Stability in real food webs: weak links in long loops. Science 296, 1120–1123 (2002).
Fox, J. & Weisberg, S. An R Companion to Applied Regression (Sage, Thousand Oaks, 2010).
Gelman, A. Scaling regression inputs by dividing by two standard deviations. Stat. Med. 27, 2865–2873 (2008).
Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biometric. J. 50, 346–363 (2008).
Zuur, A. F., Ieni, E. N., Walker, N. J., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, New York, 2009).
Acknowledgements
B.S. acknowledges the support of the German Academic Exchange Service (DAAD). A.D.B., M.P.T., U.B., B.R. and N.E. acknowledge the support of the German Centre for integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig funded by the German Research Foundation (FZT 118). A.D.B. was funded by the German Research Foundation within the framework of the Jena Experiment (FOR 1451). N.E. acknowledges funding by the German Research Foundation (DFG; Ei 862/1, Ei 862/2). This project also received support from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no 677232 to N.E.). The B4WarmED project has been funded by the US Department of Energy (Grant No. DE-FG02-07ER64456), College of Food, Agricultural and Natural Resource Sciences (CFANS), and Wilderness Research Foundation at the University of Minnesota, and the Minnesota Environment and Natural Resources Trust Fund.
Author information
Authors and Affiliations
Contributions
B.S., A.D.B., M.P.T and N.E. designed the study. P.B.R. designed and co-ordinated the B4WarmED experiment. R.L.R. and A.S. designed and implemented the warming and rainfall manipulation system. B.S., M.C., A.S. and N.E. carried out the field and laboratory work. B.S. analysed the data with inputs from A.D.B, M.P.T. and N.E. B.S., A.D.B., M.P.T. and N.E. jointly wrote the first draft, and all other authors contributed substantially to the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations
Electronic supplementary material
Supplementary Information
Supplementary Figures 1–8, Supplementary Tables 1–11, Supplementary References
Supplementary Data 1
This table contains plot-level biomass data of the first experiment. Biomasses (mg C m–2) are given for each feeding guild as well as for trophic groups (microbes, herbivores, detritivores and predators), total fauna, and the whole network
Supplementary Data 2
This table contains plot-level energy flux data of the first experiment. Energy fluxes (g C m–2 d–1) are given for each feeding guild as well as for trophic groups (microbes, herbivores, detritivores and predators), total fauna, and the whole network
Supplementary Data 3
This table contains plot-level biomass data of the second experiment. Biomasses (mg C m–2) are given for each feeding guild as well as for trophic groups (microbes, herbivores, detritivores and predators), total fauna, and the whole network
Supplementary Data 4
This table contains plot-level energy flux data of the second experiment. Energy fluxes (g C m–2 d–1) are given for each feeding guild as well as for trophic groups (microbes, herbivores, detritivores and predators), total fauna, and the whole network
Rights and permissions
About this article
Cite this article
Schwarz, B., Barnes, A.D., Thakur, M.P. et al. Warming alters energetic structure and function but not resilience of soil food webs. Nature Clim Change 7, 895–900 (2017). https://doi.org/10.1038/s41558-017-0002-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41558-017-0002-z
This article is cited by
-
Rainforest transformation reallocates energy from green to brown food webs
Nature (2024)
-
Warming causes contrasting spider behavioural responses by changing their prey size spectra
Nature Climate Change (2024)
-
Advancements in assessing soil health through functional traits and energy flow analysis of soil nematodes
Soil Ecology Letters (2024)
-
Understanding and mitigating climate change impacts on ecosystem health and functionality
Rendiconti Lincei. Scienze Fisiche e Naturali (2024)
-
Climate change and cropland management compromise soil integrity and multifunctionality
Communications Earth & Environment (2023)