Fungal colonization of plant roots is resistant to nitrogen addition and resilient to dominant species losses
Abstract
Abstract Global change drivers, such as nitrogen (N) deposition and non‐random species extinctions, may shift interactions among aboveground and belowground communities. However, tightly coupled interactions between aboveground and belowground organisms may buffer ecosystems to global change. Here, we test how four years of organic and inorganic N addition and removal of a dominant plant species, Festuca thurberi , independently and interactively influences fungal colonization patterns and performance in a co‐dominant plant species, Helianthella quinquenervis . Surprisingly, we found N addition and Festuca removal had no measurable effects on the colonization of arbuscular mycorrhizal fungi (AMF) and dark septate endophyte ( DSE ) or the performance of Helianthella seedlings grown with field‐collected inoculum in a companion greenhouse experiment. However, the proximity of Helianthella to Festuca predicted fungal colonization: DSE colonization decreased by 1% for each cm of distance Helianthella was from Festuca , although the differences in fungal inoculum potential had no effect on Helianthella seedling survival or biomass. Our results suggest that plant–fungal interactions can be resistant to N addition and resilient to the loss of dominant plant species. Additionally, our results suggest that soil legacies, mediated through surviving symbiont communities or changes in soil properties, can shape ecosystem resistancemore »
- Authors:
-
- Ecology and Evolutionary Biology University of Tennessee 569 Dabney Hall, 1416 Circle Drive Knoxville Tennessee 37996 USA, Rocky Mountain Biological Laboratory P.O. Box 519 Crested Butte Colorado 81224 USA, Ecology, Evolution, and Behavior University of Minnesota 140 Gortner Laboratory, 1479 Gortner Avenue Saint Paul Minnesota 55108 USA
- Ecology and Evolutionary Biology University of Tennessee 569 Dabney Hall, 1416 Circle Drive Knoxville Tennessee 37996 USA, Rocky Mountain Biological Laboratory P.O. Box 519 Crested Butte Colorado 81224 USA, National Socio‐Environmental Synthesis Center (SESYNC) 1 Park Place Annapolis Maryland 21401 USA
- Rocky Mountain Biological Laboratory P.O. Box 519 Crested Butte Colorado 81224 USA, Environmental Program Rubenstein School of Environment and Natural Resources University of Vermont Burlington Vermont 05405 USA, The Gund Institute for Environment The University of Vermont Burlington Vermont 05405 USA
- Rocky Mountain Biological Laboratory P.O. Box 519 Crested Butte Colorado 81224 USA, Environmental Program Rubenstein School of Environment and Natural Resources University of Vermont Burlington Vermont 05405 USA, The Gund Institute for Environment The University of Vermont Burlington Vermont 05405 USA, Rubenstein School of Environment and Natural Resources University of Vermont Burlington Vermont 05405 USA
- Publication Date:
- Research Org.:
- Univ. of Tennessee, Knoxville, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1499078
- Alternate Identifier(s):
- OSTI ID: 1499079; OSTI ID: 1500017
- Grant/Contract Number:
- DE‐SC0010562; SC0010562
- Resource Type:
- Published Article
- Journal Name:
- Ecosphere
- Additional Journal Information:
- Journal Name: Ecosphere Journal Volume: 10 Journal Issue: 3; Journal ID: ISSN 2150-8925
- Publisher:
- Wiley Blackwell (John Wiley & Sons)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES
Citation Formats
Henning, Jeremiah A., Read, Quentin D., Sanders, Nathan J., and Classen, Aimee T. Fungal colonization of plant roots is resistant to nitrogen addition and resilient to dominant species losses. United States: N. p., 2019.
Web. doi:10.1002/ecs2.2640.
Henning, Jeremiah A., Read, Quentin D., Sanders, Nathan J., & Classen, Aimee T. Fungal colonization of plant roots is resistant to nitrogen addition and resilient to dominant species losses. United States. https://doi.org/10.1002/ecs2.2640
Henning, Jeremiah A., Read, Quentin D., Sanders, Nathan J., and Classen, Aimee T. Tue .
"Fungal colonization of plant roots is resistant to nitrogen addition and resilient to dominant species losses". United States. https://doi.org/10.1002/ecs2.2640.
@article{osti_1499078,
title = {Fungal colonization of plant roots is resistant to nitrogen addition and resilient to dominant species losses},
author = {Henning, Jeremiah A. and Read, Quentin D. and Sanders, Nathan J. and Classen, Aimee T.},
abstractNote = {Abstract Global change drivers, such as nitrogen (N) deposition and non‐random species extinctions, may shift interactions among aboveground and belowground communities. However, tightly coupled interactions between aboveground and belowground organisms may buffer ecosystems to global change. Here, we test how four years of organic and inorganic N addition and removal of a dominant plant species, Festuca thurberi , independently and interactively influences fungal colonization patterns and performance in a co‐dominant plant species, Helianthella quinquenervis . Surprisingly, we found N addition and Festuca removal had no measurable effects on the colonization of arbuscular mycorrhizal fungi (AMF) and dark septate endophyte ( DSE ) or the performance of Helianthella seedlings grown with field‐collected inoculum in a companion greenhouse experiment. However, the proximity of Helianthella to Festuca predicted fungal colonization: DSE colonization decreased by 1% for each cm of distance Helianthella was from Festuca , although the differences in fungal inoculum potential had no effect on Helianthella seedling survival or biomass. Our results suggest that plant–fungal interactions can be resistant to N addition and resilient to the loss of dominant plant species. Additionally, our results suggest that soil legacies, mediated through surviving symbiont communities or changes in soil properties, can shape ecosystem resistance and resilience to disturbance and perturbations.},
doi = {10.1002/ecs2.2640},
journal = {Ecosphere},
number = 3,
volume = 10,
place = {United States},
year = {Tue Mar 12 00:00:00 EDT 2019},
month = {Tue Mar 12 00:00:00 EDT 2019}
}
https://doi.org/10.1002/ecs2.2640
Web of Science
Figures / Tables:
Works referenced in this record:
Patterns of arbuscular mycorrhiza colonisation of the roots of Hyacinthoides non-scripta after disruption of soil mycelium
journal, September 1998
- Merryweather, J. W.; Fitter, Alastair H.
- Mycorrhiza, Vol. 8, Issue 2
Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency
journal, August 2009
- Alberton, Odair; Kuyper, Thomas W.; Summerbell, Richard C.
- Plant and Soil, Vol. 328, Issue 1-2
Plant functional effects on ecosystem services
journal, December 2012
- Lavorel, Sandra
- Journal of Ecology, Vol. 101, Issue 1
A meta-analysis of plant responses to dark septate root endophytes
journal, January 2011
- Newsham, K. K.
- New Phytologist, Vol. 190, Issue 3
Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species
journal, July 2007
- Scheublin, Tanja R.; Van Logtestijn, Richard S. P.; Van Der Heijden, Marcel G. A.
- Journal of Ecology, Vol. 95, Issue 4
Plant-mycorrhizal interactions mediate plant community coexistence by altering resource demand
journal, January 2017
- Jiang, Jiang; Moore, Jessica A. M.; Priyadarshi, Anupam
- Ecology, Vol. 98, Issue 1
Arbuscular mycorrhizas in phosphate-polluted soil: interrelations between root colonization and nitrogen
journal, February 2011
- Blanke, Verena; Wagner, Markus; Renker, Carsten
- Plant and Soil, Vol. 343, Issue 1-2
Preferential allocation, physio-evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts
journal, January 2015
- Bever, James D.
- New Phytologist, Vol. 205, Issue 4
Simultaneous Inference in General Parametric Models
journal, June 2008
- Hothorn, Torsten; Bretz, Frank; Westfall, Peter
- Biometrical Journal, Vol. 50, Issue 3
Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes
journal, June 2009
- Upson, Rebecca; Read, David J.; Newsham, Kevin K.
- Mycorrhiza, Vol. 20, Issue 1
Alternative states and positive feedbacks in restoration ecology
journal, January 2004
- Suding, Katharine N.; Gross, Katherine L.; Houseman, Gregory R.
- Trends in Ecology & Evolution, Vol. 19, Issue 1
A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies
journal, July 2004
- Treseder, Kathleen K.
- New Phytologist, Vol. 164, Issue 2
Long-term effects of species loss on community properties across contrasting ecosystems
journal, May 2018
- Kardol, Paul; Fanin, Nicolas; Wardle, David A.
- Nature, Vol. 557, Issue 7707
Boreal forest plants take up organic nitrogen
journal, April 1998
- Näsholm, Torgny; Ekblad, Alf; Nordin, Annika
- Nature, Vol. 392, Issue 6679
Differential effects of two dominant plant species on community structure and invasibility in an old-field ecosystem
journal, November 2010
- Souza, Lara; Weltzin, Jake F.; Sanders, Nathan J.
- Journal of Plant Ecology, Vol. 4, Issue 3
Aboveground and Belowground Effects of Single-Tree Removals in new Zealand rain Forest
journal, May 2008
- Wardle, David A.; Wiser, Susan K.; Allen, Robert B.
- Ecology, Vol. 89, Issue 5
Biotic and abiotic predictors of fungal colonization in grasses of the Colorado Rockies
journal, February 2015
- Ranelli, Luciana B.; Hendricks, Will Q.; Lynn, Joshua S.
- Diversity and Distributions, Vol. 21, Issue 8
Ecosystem properties determined by plant functional group identity
journal, March 2010
- McLaren, Jennie R.; Turkington, Roy
- Journal of Ecology, Vol. 98, Issue 2
A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi
journal, July 1990
- McGONIGLE, T. P.; Miller, M. H.; Evans, D. G.
- New Phytologist, Vol. 115, Issue 3
A modified procedure for staining roots to detect VA mycorrhizas
journal, June 1989
- Koske, R. E.; Gemma, J. N.
- Mycological Research, Vol. 92, Issue 4
The development of mycorrhizal infection in cucumber: effects of P supply on root growth, formation of entry points and growth of infection units
journal, June 1994
- Bruce, A.; Smith, S. E.; Tester, M.
- New Phytologist, Vol. 127, Issue 3
Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi
journal, September 2009
- Powell, Jeff R.; Parrent, Jeri L.; Hart, Miranda M.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1676
Herbivores and nutrients control grassland plant diversity via light limitation
journal, March 2014
- Borer, Elizabeth T.; Seabloom, Eric W.; Gruner, Daniel S.
- Nature, Vol. 508, Issue 7497
Host-Dependent Sporulation and Species Diversity of Arbuscular Mycorrhizal Fungi in a Mown Grassland
journal, February 1996
- Bever, James D.; Morton, Joseph B.; Antonovics, Janis
- The Journal of Ecology, Vol. 84, Issue 1
Fitting Linear Mixed-Effects Models Using lme4
journal, January 2015
- Bates, Douglas; Mächler, Martin; Bolker, Ben
- Journal of Statistical Software, Vol. 67, Issue 1
Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems
journal, December 2007
- Elser, James J.; Bracken, Matthew E. S.; Cleland, Elsa E.
- Ecology Letters, Vol. 10, Issue 12
Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe
journal, August 2015
- Leff, Jonathan W.; Jones, Stuart E.; Prober, Suzanne M.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 35
Where, when and how plant-soil feedback matters in a changing world
journal, April 2016
- van der Putten, Wim H.; Bradford, Mark A.; Pernilla Brinkman, E.
- Functional Ecology, Vol. 30, Issue 7
Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi
journal, February 2002
- Hart, Miranda M.; Reader, Richard J.
- New Phytologist, Vol. 153, Issue 2
Mycorrhizal community resilience in response to experimental plant functional type removals in a woody ecosystem
journal, November 2009
- Urcelay, Carlos; Díaz, Sandra; Gurvich, Diego E.
- Journal of Ecology, Vol. 97, Issue 6
Grassland productivity limited by multiple nutrients
journal, July 2015
- Fay, Philip A.; Prober, Suzanne M.; Harpole, W. Stanley
- Nature Plants, Vol. 1, Issue 7
Patterns of Rhizosphere Microbial Community Structure Associated with Co-Occurring Plant Species
journal, December 1997
- Westover, Kristi M.; Kennedy, Ann C.; Kelley, Steven E.
- The Journal of Ecology, Vol. 85, Issue 6
Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils: COMMUNITY ASSEMBLY OF MYCORRHIZAL FUNGI
journal, March 2012
- Verbruggen, Erik; Van Der HEIJDEN, Marcel G. A.; Weedon, James T.
- Molecular Ecology, Vol. 21, Issue 10
Soil microbial communities resistant to changes in plant functional group composition
journal, January 2011
- Marshall, Carolyn B.; McLaren, Jennie R.; Turkington, Roy
- Soil Biology and Biochemistry, Vol. 43, Issue 1
Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems
journal, June 2014
- Hodge, Angela; Storer, Kate
- Plant and Soil, Vol. 386, Issue 1-2
Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non-and arbuscular mycorrhizal species access different sources of soil nitrogen
journal, January 1996
- Michelsen, Anders; Schmidt, Inger K.; Jonasson, Sven
- Oecologia, Vol. 105, Issue 1
Mycorrhizal fungal spore community structure in a manipulated prairie
journal, August 2017
- Henning, Jeremiah A.; Weiher, Evan; Lee, Tali D.
- Restoration Ecology, Vol. 26, Issue 1
The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content
journal, March 2013
- Treseder, Kathleen K.
- Plant and Soil, Vol. 371, Issue 1-2
Plant Removals in Perennial Grassland: Vegetation Dynamics, Decomposers, soil Biodiversity, and Ecosystem Properties
journal, November 1999
- Wardle, David A.; Bonner, Karen I.; Barker, Gary M.
- Ecological Monographs, Vol. 69, Issue 4
Mycorrhizal Community Dynamics Following Nitrogen Fertilization: a Cross-Site test in five Grasslands
journal, November 2007
- Egerton-Warburton, Louise M.; Johnson, Nancy Collins; Allen, Edith B.
- Ecological Monographs, Vol. 77, Issue 4
Plant neighborhood control of arbuscular mycorrhizal community composition
journal, September 2009
- Hausmann, Natasha Teutsch; Hawkes, Christine V.
- New Phytologist, Vol. 183, Issue 4
Nitrogen enrichment modifies plant community structure via changes to plant–soil feedback
journal, July 2008
- Manning, P.; Morrison, S. A.; Bonkowski, M.
- Oecologia, Vol. 157, Issue 4
Rooting theories of plant community ecology in microbial interactions
journal, August 2010
- Bever, James D.; Dickie, Ian A.; Facelli, Evelina
- Trends in Ecology & Evolution, Vol. 25, Issue 8
Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity
journal, November 1998
- van der Heijden, Marcel G. A.; Klironomos, John N.; Ursic, Margot
- Nature, Vol. 396, Issue 6706
Nitrogen Enrichment Alters Mycorrhizal Allocation at five Mesic to Semiarid Grasslands
journal, July 2003
- Johnson, Nancy Collins; Rowland, Diane L.; Corkidi, Lea
- Ecology, Vol. 84, Issue 7
Feeback between Plants and Their Soil Communities in an Old Field Community
journal, October 1994
- Bever, James D.
- Ecology, Vol. 75, Issue 7
Co-existing grass species have distinctive arbuscular mycorrhizal communities: DIVERSITY OF AM FUNGI IN GRASSLAND
journal, September 2003
- Vandenkoornhuyse, P.; Ridgway, K. P.; Watson, I. J.
- Molecular Ecology, Vol. 12, Issue 11
Mycorrhizal phenotypes and the Law of the Minimum
journal, November 2014
- Johnson, Nancy Collins; Wilson, Gail W. T.; Wilson, Jacqueline A.
- New Phytologist, Vol. 205, Issue 4