Warming alters energetic structure and function but not resilience of soil food webs
Abstract
Climate warming is predicted to alter the structure, stability, and functioning of food webs. 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–temperatemore »
- Authors:
-
[1];
[2];
[4];
[3]
- Univ. of Minnesota, Minneapolis, MN (United States); Albert-Ludwigs-Univ. Freiburg, Freiburg (Germany)
- German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig (German); Leipzig Univ., Leipzig (Germany); Univ. of Muenster, Muenster (Germany)
- German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig (German); Leipzig Univ., Leipzig (Germany)
- Univ. of Minnesota, Minneapolis, MN (United States); German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig (German)
- National Inst. of Research and Development for Biological Sciences, Cluj-Napoca (Romania). Inst. of Biological Research
- Univ. of Minnesota, Minneapolis, MN (United States); Western Sydney Univ., Penrith, NSW (Australia)
- Univ. of Minnesota, Minneapolis, MN (United States); Smithsonian Environmental Research Center, Edgewater, MD (United States)
- Univ. of Minnesota, Minneapolis, MN (United States)
- Publication Date:
- Research Org.:
- Univ. of Minnesota, Minneapolis, MN (United States)
- Sponsoring Org.:
- USDOE; German Research Foundation (DFG)
- OSTI Identifier:
- 1546788
- Grant/Contract Number:
- FG02-07ER64456; 677232
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Climate Change
- Additional Journal Information:
- Journal Volume: 7; Journal Issue: 12; Journal ID: ISSN 1758-678X
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Schwarz, Benjamin, Barnes, Andrew D., Thakur, Madhav P., Brose, Ulrich, Ciobanu, Marcel, Reich, Peter B., Rich, Roy L., Rosenbaum, Benjamin, Stefanski, Artur, and Eisenhauer, Nico. Warming alters energetic structure and function but not resilience of soil food webs. United States: N. p., 2017.
Web. doi:10.1038/s41558-017-0002-z.
Schwarz, Benjamin, Barnes, Andrew D., Thakur, Madhav P., Brose, Ulrich, Ciobanu, Marcel, Reich, Peter B., Rich, Roy L., Rosenbaum, Benjamin, Stefanski, Artur, & Eisenhauer, Nico. Warming alters energetic structure and function but not resilience of soil food webs. United States. doi:10.1038/s41558-017-0002-z.
Schwarz, Benjamin, Barnes, Andrew D., Thakur, Madhav P., Brose, Ulrich, Ciobanu, Marcel, Reich, Peter B., Rich, Roy L., Rosenbaum, Benjamin, Stefanski, Artur, and Eisenhauer, Nico. Mon .
"Warming alters energetic structure and function but not resilience of soil food webs". United States. doi:10.1038/s41558-017-0002-z. https://www.osti.gov/servlets/purl/1546788.
@article{osti_1546788,
title = {Warming alters energetic structure and function but not resilience of soil food webs},
author = {Schwarz, Benjamin and Barnes, Andrew D. and Thakur, Madhav P. and Brose, Ulrich and Ciobanu, Marcel and Reich, Peter B. and Rich, Roy L. and Rosenbaum, Benjamin and Stefanski, Artur and Eisenhauer, Nico},
abstractNote = {Climate warming is predicted to alter the structure, stability, and functioning of food webs. 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.},
doi = {10.1038/s41558-017-0002-z},
journal = {Nature Climate Change},
number = 12,
volume = 7,
place = {United States},
year = {2017},
month = {11}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 12 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Studies On the Nematode Fauna of an Acid Forest Soil: Spatial Distribution and Extraction
journal, January 1995
- Ruess, Liliane
- Nematologica, Vol. 41, Issue 1-4
Phylogenetic grouping, curvature and metabolic scaling in terrestrial invertebrates: Invertebrate metabolism
journal, July 2011
- Ehnes, Roswitha B.; Rall, Björn C.; Brose, Ulrich
- Ecology Letters, Vol. 14, Issue 10
Soil food web structure during ecosystem development after land abandonment
journal, May 2008
- Holtkamp, Remko; Kardol, Paul; van der Wal, Annemieke
- Applied Soil Ecology, Vol. 39, Issue 1
Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems: WARMING ALTERS COMMUNITY SIZE STRUCTURE
journal, October 2010
- Yvon-Durocher, Gabriel; Montoya, JosÉ M.; Trimmer, Mark
- Global Change Biology, Vol. 17, Issue 4
Cross-ecosystem differences in stability and the principle of energy flux: Cross-ecosystem differences in stability
journal, June 2011
- Rip, J. M. K.; McCann, K. S.
- Ecology Letters, Vol. 14, Issue 8
Effects of soil temperature and moisture on the feeding activity of soil animals as determined by the bait-lamina test
journal, May 2008
- Gongalsky, Konstantin B.; Persson, Tryggve; Pokarzhevskii, Andrei D.
- Applied Soil Ecology, Vol. 39, Issue 1
Simultaneous Inference in General Parametric Models
journal, June 2008
- Hothorn, Torsten; Bretz, Frank; Westfall, Peter
- Biometrical Journal, Vol. 50, Issue 3
Utilization of organic materials in soil aggregates by bacteria and fungi
journal, January 1978
- Adu, J. K.; Oades, J. M.
- Soil Biology and Biochemistry, Vol. 10, Issue 2
Environmental warming alters food-web structure and ecosystem function
journal, November 1999
- Petchey, Owen L.; McPhearson, P. Timon; Casey, Timothy M.
- Nature, Vol. 402, Issue 6757
Effects of Size and Temperature on Metabolic Rate
journal, September 2001
- Gillooly, J. F.
- Science, Vol. 293, Issue 5538
Organic textile dye improves the visual assessment of the bait-lamina test
journal, October 2014
- Eisenhauer, Nico; Wirsch, Daniela; Cesarz, Simone
- Applied Soil Ecology, Vol. 82
Land use alters the resistance and resilience of soil food webs to drought
journal, January 2012
- de Vries, Franciska T.; Liiri, Mira E.; Bjørnlund, Lisa
- Nature Climate Change, Vol. 2, Issue 4
Ecological stability in response to warming
journal, February 2014
- Fussmann, Katarina E.; Schwarzmüller, Florian; Brose, Ulrich
- Nature Climate Change, Vol. 4, Issue 3
Drought alters the structure and functioning of complex food webs
journal, September 2012
- Ledger, Mark E.; Brown, Lee E.; Edwards, François K.
- Nature Climate Change, Vol. 3, Issue 3
Patterns in the Fate of Production in Plant Communities
journal, October 1999
- Cebrian, Just
- The American Naturalist, Vol. 154, Issue 4
Interactive effects of warming, eutrophication and size structure: impacts on biodiversity and food-web structure
journal, November 2015
- Binzer, Amrei; Guill, Christian; Rall, Björn C.
- Global Change Biology, Vol. 22, Issue 1
Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15N/14N and 13C/12C)
journal, June 2009
- Pollierer, Melanie M.; Langel, Reinhard; Scheu, Stefan
- Soil Biology and Biochemistry, Vol. 41, Issue 6
Managing uncertainty in soil carbon feedbacks to climate change
journal, July 2016
- Bradford, Mark A.; Wieder, William R.; Bonan, Gordon B.
- Nature Climate Change, Vol. 6, Issue 8
The relation of energy and organic carbon in aquatic invertebrates1: Energy and organic carbon
journal, September 1976
- Salonen, Kalevi; Sarvala, Jouko; Hakala, Ilpo
- Limnology and Oceanography, Vol. 21, Issue 5
Warming magnifies predation and reduces prey coexistence in a model litter arthropod system
journal, March 2017
- Thakur, Madhav P.; Künne, Tom; Griffin, John N.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 284, Issue 1851
Survival of two ecologically distinct bacteria (Flavobacterium and arthrobacter) in unplanted and rhizosphere soil: Field studies
journal, January 1992
- Thompson, I. P.; Young, C. S.; Cook, K. A.
- Soil Biology and Biochemistry, Vol. 24, Issue 1
The Ecology of Nematodes in Agroecosystems
journal, September 1985
- Freckman, D. W.; Caswell, E. P.
- Annual Review of Phytopathology, Vol. 23, Issue 1
A critique of the microbial metabolic quotient (qCO2) as a bioindicator of disturbance and ecosystem development
journal, December 1995
- Wardle, D. A.; Ghani, A.
- Soil Biology and Biochemistry, Vol. 27, Issue 12
Climate change effects on soil microarthropod abundance and community structure
journal, January 2011
- Kardol, Paul; Reynolds, W. Nicholas; Norby, Richard J.
- Applied Soil Ecology, Vol. 47, Issue 1
Simulation of Nitrogen Mineralization in the Below-Ground Food Webs of Two Winter Wheat Fields
journal, January 1993
- Ruiter, P. C. De; Moore, J. C.; Zwart, K. B.
- The Journal of Applied Ecology, Vol. 30, Issue 1
Effects of environmental warming and drought on size-structured soil food webs
journal, December 2013
- Lang, Birgit; Rall, Björn C.; Scheu, Stefan
- Oikos, Vol. 123, Issue 10
A bioenergetic framework for the temperature dependence of trophic interactions
journal, June 2014
- Gilbert, Benjamin; Tunney, Tyler D.; McCann, Kevin S.
- Ecology Letters, Vol. 17, Issue 8
Direct contribution by soil arthropods to nutrient availability through body and faecal nutrient content
journal, October 1992
- Teuben, A.; Verhoef, H. A.
- Biology and Fertility of Soils, Vol. 14, Issue 2
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
journal, May 2000
- Scheu, S.; Falca, M.
- Oecologia, Vol. 123, Issue 2
Climate remains an important driver of post-European vegetation change in the eastern United States
journal, December 2014
- Pederson, Neil; D'Amato, Anthony W.; Dyer, James M.
- Global Change Biology, Vol. 21, Issue 6
Energetics, Patterns of Interaction Strengths, and Stability in Real Ecosystems
journal, September 1995
- de Ruiter, P. C.; Neutel, A. -M.; Moore, J. C.
- Science, Vol. 269, Issue 5228
An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C
journal, July 1997
- Beck, T.; Joergensen, R. G.; Kandeler, E.
- Soil Biology and Biochemistry, Vol. 29, Issue 7
Fungal-feeding habits of six nematode isolates in the genus Filenchus
journal, June 2005
- Okada, Hiroaki; Harada, Hiroki; Kadota, Ikuo
- Soil Biology and Biochemistry, Vol. 37, Issue 6
Long-term forest soil warming alters microbial communities in temperate forest soils
journal, February 2015
- DeAngelis, Kristen M.; Pold, Grace; Topçuoğlu, Begüm D.
- Frontiers in Microbiology, Vol. 6
Scaling regression inputs by dividing by two standard deviations
journal, January 2008
- Gelman, Andrew
- Statistics in Medicine, Vol. 27, Issue 15
Nematode community shifts in response to experimental warming and canopy conditions are associated with plant community changes in the temperate-boreal forest ecotone
journal, March 2014
- Thakur, Madhav Prakash; Reich, Peter B.; Fisichelli, Nicholas A.
- Oecologia, Vol. 175, Issue 2
A physiological method for the quantitative measurement of microbial biomass in soils
journal, January 1978
- Anderson, J. P. E.; Domsch, K. H.
- Soil Biology and Biochemistry, Vol. 10, Issue 3
Thermal adaptation of soil microbial respiration to elevated temperature
journal, December 2008
- Bradford, Mark A.; Davies, Christian A.; Frey, Serita D.
- Ecology Letters, Vol. 11, Issue 12
Soil meso- and macrofauna in two agricultural systems: factors affecting population dynamics and evaluation of their role in carbon and nitrogen dynamics
journal, November 1994
- Didden, W. A. M.; Marinissen, J. C. Y.; Vreeken-Buijs, M. J.
- Agriculture, Ecosystems & Environment, Vol. 51, Issue 1-2
Stability in Real Food Webs: Weak Links in Long Loops
journal, May 2002
- Neutel, A. -M.
- Science, Vol. 296, Issue 5570
Reconciling complexity with stability in naturally assembling food webs
journal, October 2007
- Neutel, Anje-Margriet; Heesterbeek, Johan A. P.; van de Koppel, Johan
- Nature, Vol. 449, Issue 7162
Invertebrate body sizes from Marion Island
journal, June 2001
- Mercer, Richard D.; Gabriel, A. G. A.; Barendse, J.
- Antarctic Science, Vol. 13, Issue 2
Temperature, predator-prey interaction strength and population stability: TEMPERATURE AND INTERACTION STRENGTH
journal, November 2009
- Rall, BjÖRn C.; Vucic-Pestic, Olivera; Ehnes, Roswitha B.
- Global Change Biology, Vol. 16, Issue 8
Community food web, decomposition and nitrogen mineralisation in a stratified Scots pine forest soil
journal, July 2001
- Berg, Matty; de Ruiter, Peter; Didden, Wim
- Oikos, Vol. 94, Issue 1
Consequences of tropical land use for multitrophic biodiversity and ecosystem functioning
journal, October 2014
- Barnes, Andrew D.; Jochum, Malte; Mumme, Steffen
- Nature Communications, Vol. 5, Issue 1
Soil biodiversity and human health
journal, November 2015
- Wall, Diana H.; Nielsen, Uffe N.; Six, Johan
- Nature, Vol. 528, Issue 7580
Works referencing / citing this record:
Horizontal and vertical diversity jointly shape food web stability against small and large perturbations
journal, May 2019
- Zhao, Qinghua; Van den Brink, Paul J.; Carpentier, Camille
- Ecology Letters, Vol. 22, Issue 7
A simple model predicts how warming simplifies wild food webs
journal, July 2019
- O’Gorman, Eoin J.; Petchey, Owen L.; Faulkner, Katy J.
- Nature Climate Change, Vol. 9, Issue 8
A simple model predicts how warming simplifies wild food webs
journal, July 2019
- O’Gorman, Eoin J.; Petchey, Owen L.; Faulkner, Katy J.
- Nature Climate Change, Vol. 9, Issue 8
Horizontal and vertical diversity jointly shape food web stability against small and large perturbations
journal, May 2019
- Zhao, Qinghua; Van den Brink, Paul J.; Carpentier, Camille
- Ecology Letters, Vol. 22, Issue 7
Eco-Evolutionary Origins of Diverse Abundance, Biomass, and Trophic Structures in Food Webs
journal, February 2019
- Gibert, Jean P.; Yeakel, Justin D.
- Frontiers in Ecology and Evolution, Vol. 7
Exotic earthworms maintain soil biodiversity by altering bottom-up effects of plants on the composition of soil microbial groups and nematode communities
journal, January 2019
- Shao, Yuanhu; Zhang, Weixin; Eisenhauer, Nico
- Biology and Fertility of Soils, Vol. 55, Issue 3
Biodiversity of intertidal food webs in response to warming across latitudes
journal, February 2020
- Gauzens, Benoit; Rall, Björn C.; Mendonça, Vanessa
- Nature Climate Change, Vol. 10, Issue 3
Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems
journal, November 2019
- Pugnaire, Francisco I.; Morillo, José A.; Peñuelas, Josep
- Science Advances, Vol. 5, Issue 11
Biotic interactions, community assembly, and eco-evolutionary dynamics as drivers of long-term biodiversity–ecosystem functioning relationships
journal, October 2019
- Eisenhauer, Nico; Bonkowski, Michael; Brose, Ulrich
- Research Ideas and Outcomes, Vol. 5