Warming reverses top-down effects of predators on belowground ecosystem function in Arctic tundra
Abstract
Predators can disproportionately impact the structure and function of ecosystems relative to their biomass. These effects may be exacerbated under warming in ecosystems like the Arctic, where the number and diversity of predators are low and small shifts in community interactions can alter carbon cycle feedbacks. Here, we show that warming alters the effects of wolf spiders, a dominant tundra predator, on belowground litter decomposition. Specifically, while high densities of wolf spiders result in faster litter decomposition under ambient temperatures, they result, instead, in slower decomposition under warming. Higher spider densities are also associated with elevated levels of available soil nitrogen, potentially benefiting plant production. Changes in decomposition rates under increased wolf spider densities are accompanied by trends toward fewer fungivorous Collembola under ambient temperatures and more Collembola under warming, suggesting that Collembola mediate the indirect effects of wolf spiders on decomposition. The unexpected reversal of wolf spider effects on Collembola and decomposition suggest that in some cases, warming does not simply alter the strength of top-down effects but, instead, induces a different trophic cascade altogether. Our results indicate that climate change-induced effects on predators can cascade through other trophic levels, alter critical ecosystem functions, and potentially lead to climatemore »
- Publication Date:
- Research Org.:
- Univ. of Tennessee, Knoxville, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1461247
- Alternate Identifier(s):
- OSTI ID: 1501423
- Grant/Contract Number:
- SC0010562
- Resource Type:
- Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 115 Journal Issue: 32; Journal ID: ISSN 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES
Citation Formats
Koltz, Amanda M., Classen, Aimée T., and Wright, Justin P. Warming reverses top-down effects of predators on belowground ecosystem function in Arctic tundra. United States: N. p., 2018.
Web. doi:10.1073/pnas.1808754115.
Koltz, Amanda M., Classen, Aimée T., & Wright, Justin P. Warming reverses top-down effects of predators on belowground ecosystem function in Arctic tundra. United States. https://doi.org/10.1073/pnas.1808754115
Koltz, Amanda M., Classen, Aimée T., and Wright, Justin P. Mon .
"Warming reverses top-down effects of predators on belowground ecosystem function in Arctic tundra". United States. https://doi.org/10.1073/pnas.1808754115.
@article{osti_1461247,
title = {Warming reverses top-down effects of predators on belowground ecosystem function in Arctic tundra},
author = {Koltz, Amanda M. and Classen, Aimée T. and Wright, Justin P.},
abstractNote = {Predators can disproportionately impact the structure and function of ecosystems relative to their biomass. These effects may be exacerbated under warming in ecosystems like the Arctic, where the number and diversity of predators are low and small shifts in community interactions can alter carbon cycle feedbacks. Here, we show that warming alters the effects of wolf spiders, a dominant tundra predator, on belowground litter decomposition. Specifically, while high densities of wolf spiders result in faster litter decomposition under ambient temperatures, they result, instead, in slower decomposition under warming. Higher spider densities are also associated with elevated levels of available soil nitrogen, potentially benefiting plant production. Changes in decomposition rates under increased wolf spider densities are accompanied by trends toward fewer fungivorous Collembola under ambient temperatures and more Collembola under warming, suggesting that Collembola mediate the indirect effects of wolf spiders on decomposition. The unexpected reversal of wolf spider effects on Collembola and decomposition suggest that in some cases, warming does not simply alter the strength of top-down effects but, instead, induces a different trophic cascade altogether. Our results indicate that climate change-induced effects on predators can cascade through other trophic levels, alter critical ecosystem functions, and potentially lead to climate feedbacks with important global implications. Moreover, given the expected increase in wolf spider densities with climate change, our findings suggest that the observed cascading effects of this common predator on detrital processes could potentially buffer concurrent changes in decomposition rates.},
doi = {10.1073/pnas.1808754115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 32,
volume = 115,
place = {United States},
year = {2018},
month = {7}
}
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https://doi.org/10.1073/pnas.1808754115
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Works referenced in this record:
Traits explain the responses of a sub-arctic Collembola community to climate manipulation
journal, February 2011
- Makkonen, Marika; Berg, Matty P.; van Hal, Jurgen R.
- Soil Biology and Biochemistry, Vol. 43, Issue 2
Microorganisms and climate change: terrestrial feedbacks and mitigation options
journal, October 2010
- Singh, Brajesh K.; Bardgett, Richard D.; Smith, Pete
- Nature Reviews Microbiology, Vol. 8, Issue 11
Vulnerability of Permafrost Carbon to Climate Change: Implications for the Global Carbon Cycle
journal, September 2008
- Schuur, Edward A. G.; Bockheim, James; Canadell, Josep G.
- BioScience, Vol. 58, Issue 8
Tight coupling between leaf area index and foliage N content in arctic plant communities
journal, November 2004
- van Wijk, Mark T.; Williams, Mathew; Shaver, Gaius R.
- Oecologia, Vol. 142, Issue 3
Short-term herbivory has long-term consequences in warmed and ambient high Arctic tundra
journal, January 2017
- Little, Chelsea J.; Cutting, Helen; Alatalo, Juha
- Environmental Research Letters, Vol. 12, Issue 2
Extensive niche overlap among the dominant arthropod predators of the High Arctic
journal, February 2015
- Wirta, Helena K.; Weingartner, Elisabeth; Hambäck, Peter A.
- Basic and Applied Ecology, Vol. 16, Issue 1
Community and ecosystem responses to recent climate change
journal, July 2010
- Walther, Gian-Reto
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1549
CLIMATE CHANGE: Permafrost and the Global Carbon Budget
journal, June 2006
- Zimov, S. A.
- Science, Vol. 312, Issue 5780
Clutch Size in Spiders: Is More Better?
journal, February 1994
- Marshall, S. D.; Gittleman, J. L.
- Functional Ecology, Vol. 8, Issue 1
Soil fungi: Relationships between hyphal activity and staining with fluorescein diacetate
journal, January 1984
- Ingham, E. R.; Klein, D. A.
- Soil Biology and Biochemistry, Vol. 16, Issue 3
Combined effects of elevated temperatures and reduced leaf litter quality on the life-history parameters of a saprophagous macroarthropod
journal, January 2009
- David, Jean-Francois; Gillon, Dominique
- Global Change Biology, Vol. 15, Issue 1
Contrasting Trophic Cascades Generated by a Community of Generalist Predators
journal, June 2001
- Snyder, William E.; Wise, David H.
- Ecology, Vol. 82, Issue 6
Effects on the Structure of Arctic Ecosystems in the Short- and Long-term Perspectives
journal, November 2004
- Callaghan, Terry V.; Björn, Lars Olof; Chernov, Yuri
- AMBIO: A Journal of the Human Environment, Vol. 33, Issue 7
Species Interactions Reverse Grassland Responses to Changing Climate
journal, February 2007
- Suttle, K. B.; Thomsen, M. A.; Power, M. E.
- Science, Vol. 315, Issue 5812
Large predators and trophic cascades in terrestrial ecosystems of the western United States
journal, November 2009
- Beschta, Robert L.; Ripple, William J.
- Biological Conservation, Vol. 142, Issue 11
Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization
journal, September 2004
- Mack, Michelle C.; Schuur, Edward A. G.; Bret-Harte, M. Syndonia
- Nature, Vol. 431, Issue 7007
What Determines the Strength of a Trophic Cascade?
journal, February 2005
- Borer, E. T.; Seabloom, E. W.; Shurin, J. B.
- Ecology, Vol. 86, Issue 2
Ecosystem feedbacks and cascade processes: understanding their role in the responses of Arctic and alpine ecosystems to environmental change
journal, May 2009
- Wookey, Philip A.; Aerts, Rien; Bardgett, Richard D.
- Global Change Biology, Vol. 15, Issue 5
Long-term warming restructures Arctic tundra without changing net soil carbon storage
journal, May 2013
- Sistla, Seeta A.; Moore, John C.; Simpson, Rodney T.
- Nature, Vol. 497, Issue 7451
Water availability directly determines per capita consumption at two trophic levels
journal, June 2009
- McCluney, Kevin E.; Sabo, John L.
- Ecology, Vol. 90, Issue 6
Functional shifts of grassland soil communities in response to soil warming
journal, February 2009
- Briones, María Jesús Iglesias; Ostle, Nicholas J.; McNamara, Niall P.
- Soil Biology and Biochemistry, Vol. 41, Issue 2
Intra-guild predation relaxes natural enemy impacts on herbivore populations
journal, February 2003
- Finke, Deborah L.; Denno, Robert F.
- Ecological Entomology, Vol. 28, Issue 1
Global change and species interactions in terrestrial ecosystems
journal, December 2008
- Tylianakis, Jason M.; Didham, Raphael K.; Bascompte, Jordi
- Ecology Letters, Vol. 11, Issue 12
Plants and generalist predators as links between the below-ground and above-ground system
journal, January 2001
- Scheu, Stefan
- Basic and Applied Ecology, Vol. 2, Issue 1
Wandering spiders limit densities of a major microbi-detritivore in the forest-floor food web
journal, March 2004
- Wise, David H.
- Pedobiologia, Vol. 48, Issue 2
Top-Down is Bottom-Up: does Predation in the Rhizosphere Regulate Aboveground Dynamics?
journal, April 2003
- Moore, John C.; McCann, Kevin; Setälä, Heikki
- Ecology, Vol. 84, Issue 4
Climate change and sexual size dimorphism in an Arctic spider
journal, April 2009
- Høye, Toke Thomas; Hammel, Jörg U.; Fuchs, Thomas
- Biology Letters, Vol. 5, Issue 4
Metabolic costs of the predation strategy of the spider Pardosa amentata (Clerck) (Lycosidae)
journal, January 1977
- Ford, Michael J.
- Oecologia, Vol. 28, Issue 4
Unexpected indirect effect of spiders on the rate of litter disappearance in a deciduous forest
journal, March 2004
- Lawrence, Kendra L.; Wise, David H.
- Pedobiologia, Vol. 48, Issue 2
Productivity and Trophic-Level Biomasses in a Microbial-Based Soil Food Web
journal, May 1998
- Mikola, Juha; Setälä, Heikki; Setala, Heikki
- Oikos, Vol. 82, Issue 1
Global Change and Arctic Ecosystems: Conclusions and Predictions from Experiments with Terrestrial Invertebrates on Spitsbergen
journal, August 1998
- Hodkinson, Ian D.; Webb, N. R.; Bale, J. S.
- Arctic and Alpine Research, Vol. 30, Issue 3
Warming effects on consumption and intraspecific interference competition depend on predator metabolism: Temperature effects on interference competition
journal, November 2011
- Lang, Birgit; Rall, Björn C.; Brose, Ulrich
- Journal of Animal Ecology, Vol. 81, Issue 3
Fear of predation alters soil carbon dioxide flux and nitrogen content
journal, June 2014
- Sitvarin, Michael I.; Rypstra, Ann L.
- Biology Letters, Vol. 10, Issue 6
Rainfall and hydrological stability alter the impact of top predators on food web structure and function
journal, July 2016
- Marino, Nicholas A. C.; Srivastava, Diane S.; MacDonald, A. Andrew M.
- Global Change Biology, Vol. 23, Issue 2
The Circumpolar Arctic vegetation map
journal, February 2005
- Walker, Donald A.; Raynolds, Martha K.; Daniëls, Fred J. A.
- Journal of Vegetation Science, Vol. 16, Issue 3
Highly consistent effects of plant litter identity and functional traits on decomposition across a latitudinal gradient
journal, June 2012
- Makkonen, Marika; Berg, Matty P.; Handa, I. Tanya
- Ecology Letters, Vol. 15, Issue 9
Bacterial and fungal abundance and biomass in conventional and no-tillage agroecosystems along two climatic gradients
journal, April 1999
- Frey, S. D.; Elliott, E. T.; Paustian, K.
- Soil Biology and Biochemistry, Vol. 31, Issue 4
The importance of intraguild predation in predicting emergent multiple predator effects
journal, October 2014
- Sitvarin, Michael I.; Rypstra, Ann L.
- Ecology, Vol. 95, Issue 10
Utilization of prey from the decomposer system by generalist predators of grassland
journal, December 2007
- Oelbermann, Katja; Langel, Reinhard; Scheu, Stefan
- Oecologia, Vol. 155, Issue 3
Sensitivity of the carbon cycle in the Arctic to climate change
journal, November 2009
- McGuire, A. David; Anderson, Leif G.; Christensen, Torben R.
- Ecological Monographs, Vol. 79, Issue 4
Impacts of Grazing and Climate Warming on C Pools and Decomposition Rates in Arctic Environments
journal, January 2012
- Sjögersten, Sofie; van der Wal, René; Woodin, Sarah J.
- Ecosystems, Vol. 15, Issue 3
Spider predation on forest-floor Collembola and evidence for indirect effects on decomposition
journal, January 2000
- Lawrence, Kendra L.; Wise, David H.
- Pedobiologia, Vol. 44, Issue 1
Effects of experimental temperature elevation on high-arctic soil microarthropod populations
journal, February 1996
- Coulson, S. J.; Hodkinson, I. D.; Wooley, C.
- Polar Biology, Vol. 16, Issue 2
No detectable trophic cascade in a high-Arctic arthropod food web
journal, November 2015
- Visakorpi, Kristiina; Wirta, Helena K.; Ek, Malin
- Basic and Applied Ecology, Vol. 16, Issue 7
Predators have Large Effects on Ecosystem Properties by Changing Plant Diversity, not Plant Biomass
journal, June 2006
- Schmitz, Oswald J.
- Ecology, Vol. 87, Issue 6
The detritus-based microbial-invertebrate food web contributes disproportionately to carbon and nitrogen cycling in the Arctic
journal, September 2017
- Koltz, Amanda M.; Asmus, Ashley; Gough, Laura
- Polar Biology, Vol. 41, Issue 8
Spider foraging strategy affects trophic cascades under natural and drought conditions
journal, July 2015
- Liu, Shengjie; Chen, Jin; Gan, Wenjin
- Scientific Reports, Vol. 5, Issue 1
Terrestrial Trophic Cascades: How Much Do They Trickle?
journal, March 2001
- Halaj, Juraj; Wise, David H.
- The American Naturalist, Vol. 157, Issue 3
Arctic arthropod assemblages in habitats of differing shrub dominance
journal, February 2013
- Rich, Matthew E.; Gough, Laura; Boelman, Natalie T.
- Ecography, Vol. 36, Issue 9
Arthropod Regulation of Micro- and Mesobiota in Below-Ground Detrital Food Webs
journal, January 1988
- Moore, J. C.; Walter, D. E.; Hunt, H. W.
- Annual Review of Entomology, Vol. 33, Issue 1
Integrated Regional Changes in Arctic Climate Feedbacks: Implications for the Global Climate System
journal, November 2006
- McGuire, A. David; Chapin, F. S.; Walsh, John E.
- Annual Review of Environment and Resources, Vol. 31, Issue 1
Population- and ecosystem-level effects of predation on microbial-feeding nematodes
journal, August 1999
- Laakso, Jouni; Setälä, Heikki
- Oecologia, Vol. 120, Issue 2
Temperature and prey capture: opposite relationships in two predator taxa
journal, April 2008
- Kruse, Peter Dalgas; Toft, SØRen; Sunderland, Keith D.
- Ecological Entomology, Vol. 33, Issue 2
Phylogenetic reconstruction of the wolf spiders (Araneae: Lycosidae) using sequences from the 12S rRNA, 28S rRNA, and NADH1 genes: Implications for classification, biogeography, and the evolution of web building behavior
journal, March 2006
- Murphy, Nicholas P.; Framenau, Volker W.; Donnellan, Stephen C.
- Molecular Phylogenetics and Evolution, Vol. 38, Issue 3
A test of the hierarchical model of litter decomposition
journal, November 2017
- Bradford, Mark A.; Veen, G. F.; Bonis, Anne
- Nature Ecology & Evolution, Vol. 1, Issue 12
The freezer defrosting: global warming and litter decomposition rates in cold biomes
journal, May 2006
- Aerts, R.
- Journal of Ecology, Vol. 94, Issue 4
Large herbivores limit CO2 uptake and suppress carbon cycle responses to warming in West Greenland
journal, September 2011
- Cahoon, Sean M. P.; Sullivan, Patrick F.; Post, Eric
- Global Change Biology, Vol. 18, Issue 2
Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming
journal, April 2015
- Tveit, Alexander Tøsdal; Urich, Tim; Frenzel, Peter
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 19
Soil organic carbon pools in the northern circumpolar permafrost region: SOIL ORGANIC CARBON POOLS
journal, June 2009
- Tarnocai, C.; Canadell, J. G.; Schuur, E. A. G.
- Global Biogeochemical Cycles, Vol. 23, Issue 2
Predator contributions to belowground responses to warming
journal, September 2016
- Maran, A. M.; Pelini, S. L.
- Ecosphere, Vol. 7, Issue 9
Predicted climate change alters the indirect effect of predators on an ecosystem process
journal, October 2006
- Lensing, J. R.; Wise, D. H.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 42
Fear of Predation Slows Plant-Litter Decomposition
journal, June 2012
- Hawlena, D.; Strickland, M. S.; Bradford, M. A.
- Science, Vol. 336, Issue 6087
The nature of spatial transitions in the Arctic
journal, December 2004
- Epstein, H. E.; Beringer, J.; Gould, W. A.
- Journal of Biogeography, Vol. 31, Issue 12
The Circumpolar Arctic vegetation map
journal, January 2005
- Walker, Donald A.; Raynolds, Martha K.; Daniëls, Fred J. A.
- Journal of Vegetation Science, Vol. 16, Issue 3
Works referencing / citing this record:
Body size mediates the relationship between spider (Arachnida: Araneae) assemblage composition and prey consumption rate: results of a mesocosm experiment in the Yukon, Canada
journal, February 2019
- Turney, Shaun; Buddle, Chris M.
- Oecologia, Vol. 189, Issue 3
Temperature directly and indirectly influences food web structure
journal, March 2019
- Gibert, Jean P.
- Scientific Reports, Vol. 9, Issue 1
Field exclusion of large soil predators impacts lower trophic levels and decreases leaf‐litter decomposition in dry forests
journal, September 2019
- Melguizo‐Ruiz, Nereida; Jiménez‐Navarro, Gerardo; De Mas, Eva
- Journal of Animal Ecology, Vol. 89, Issue 2
Flexibility in a changing arctic food web: Can rough‐legged buzzards cope with changing small rodent communities?
journal, September 2019
- Fufachev, Ivan A.; Ehrich, Dorothee; Sokolova, Natalia A.
- Global Change Biology, Vol. 25, Issue 11
Dominant Arctic Predator Is Free of Major Parasitoid at Northern Edge of Its Range
journal, July 2019
- Koltz, Amanda M.; Culler, Lauren E.; Bowden, Joseph J.
- Frontiers in Ecology and Evolution, Vol. 7