Arbuscular mycorrhizal fungal response to fire and urbanization in the Great Smoky Mountains National Park

Kivlin, Stephanie N.; Harpe, V. Rosanne; Turner, Jackson H.; Moore, Jessica M.; Moorhead, Leigh C.; Beals, Kendall K.; Hubert, Mali M.; Papeş, Monica; Schweitzer, Jennifer A.

doi:10.1525/elementa.2021.00037

Title: Arbuscular mycorrhizal fungal response to fire and urbanization in the Great Smoky Mountains National Park

Journal Article · Fri Dec 10 00:00:00 EST 2021 · Elementa

DOI:https://doi.org/10.1525/elementa.2021.00037· OSTI ID:1840197

Kivlin, Stephanie N. ^[1]; Harpe, V. Rosanne ^[1]; Turner, Jackson H. ^[1]; Moore, Jessica M. ^[2]; Moorhead, Leigh C. ^[3]; Beals, Kendall K. ^[1]; Hubert, Mali M. ^[1]; Papeş, Monica ^[1]; Schweitzer, Jennifer A. ^[1]

Univ. of Tennessee, Knoxville, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States); US Environmental Protection Agency (EPA), Research Triangle Park, NC (United States). Office of Research and Development, Center for Public Health and Environmental Assessment

Wildfires are increasing in frequency and intensity as drier and warmer climates increase plant detrital fuel loads. At the same time, increases in urbanization position 9% of fire-prone land within the United States at the wildland–urban interface. While rarely studied, the compounded effects of urbanization and wildfires may have unknown synergistically negative effects on ecosystems. Previous studies at the wildland–urban interface often focus on aboveground plant communities, but belowground ecosystems may also be affected by this double disturbance. In particular, it is unclear how much fire and urbanization independently or interactively affect nutritional symbioses such as those between arbuscular mycorrhizal (AM) fungi and the majority of terrestrial plants. In November 2016, extreme drought conditions and long-term fire suppression combined to create a wildfire within the Great Smoky Mountains National Park and the neighboring exurban city of Gatlinburg, TN. To understand how the double disturbance of urbanization and fire affected AM fungal communities, we collected fine roots from the 5 dominant understory species in September 2018 at each of 18 sites spanning 3 burn severities in both exurban and natural sites. Despite large variation in burn severity, plant species identity had the largest influence on AM fungi. AM fungal colonization, richness, and composition all varied most among plant species. Fire and urbanization did influence some AM fungal metrics; colonization was lower in burned sites and composition was more variable among exurban locations. There were no interactions among burn severity and urbanization on AM fungi. Our results point to the large influence of plant species identity structuring this obligate nutritional symbiosis regardless of disturbance regime. Therefore, the majority of AM fungal taxa may be buffered from fire-induced ecosystem changes if plant community composition largely remains intact, plant species life history traits allow for AM fungal persistence after fire disturbance, and/or nearby undisturbed habitat can act as an inoculum source for recolonization following fires. Thus, it is critical to maintain natural, undisturbed habitats interspersed within the wildland–urban interface.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1840197

Journal Information:: Elementa, Vol. 9, Issue 1; ISSN 2325-1026

Publisher:: University of California PressCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

Arbuscular mycorrhiza: the mother of plant root endosymbioses Parniske, Martin Nature Reviews Microbiology, Vol. 6, Issue 10 https://doi.org/10.1038/nrmicro1987	journal	October 2008
Reconciling disparate responses to grazing in the arbuscular mycorrhizal symbiosis van der Heyde, Mieke; Abbott, Lynette K.; Gehring, Catherine Rhizosphere, Vol. 11 https://doi.org/10.1016/j.rhisph.2019.100167	journal	September 2019
Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest: AM DIVERSITY IN A TROPICAL FOREST Husband, R.; Herre, E. A.; Turner, S. L. Molecular Ecology, Vol. 11, Issue 12 https://doi.org/10.1046/j.1365-294X.2002.01647.x	journal	December 2002
Effects of land use on arbuscular mycorrhizal fungal communities in Estonia Sepp, Siim-Kaarel; Jairus, Teele; Vasar, Martti Mycorrhiza, Vol. 28, Issue 3 https://doi.org/10.1007/s00572-018-0822-3	journal	January 2018
Codependency between plant and arbuscular mycorrhizal fungal communities: what is the evidence? Kokkoris, Vasilis; Lekberg, Ylva; Antunes, Pedro M. New Phytologist, Vol. 228, Issue 3 https://doi.org/10.1111/nph.16676	journal	June 2020
Modeling climate change, urbanization, and fire effects on Pinus palustris ecosystems of the southeastern U.S. Costanza, Jennifer K.; Terando, Adam J.; McKerrow, Alexa J. Journal of Environmental Management, Vol. 151 https://doi.org/10.1016/j.jenvman.2014.12.032	journal	March 2015
The Demise of Fire and “Mesophication” of Forests in the Eastern United States Nowacki, Gregory J.; Abrams, Marc D. BioScience, Vol. 58, Issue 2 https://doi.org/10.1641/B580207	journal	February 2008
Climatic Change, Wildfire, and Conservation McKENZIE, Donald; Gedalof, Ze'Ev; Peterson, David L. Conservation Biology, Vol. 18, Issue 4 https://doi.org/10.1111/j.1523-1739.2004.00492.x	journal	August 2004
The Effect of Fire, Mowing and Fertilizer Amendment on Arbuscular Mycorrhizas in Tallgrass Prairie Eom, Ahn-Heum; Hartnett, David C.; Wilson, Gail W. T. The American Midland Naturalist, Vol. 142, Issue 1 https://doi.org/10.1674/0003-0031(1999)142[0055:TEOFMA]2.0.CO;2	journal	July 1999
Urban stress is associated with variation in microbial species composition—but not richness—in Manhattan Reese, Aspen T.; Savage, Amy; Youngsteadt, Elsa The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.152	journal	September 2015
Fire regimes for pine-grassland communities in the southeastern United States Waldrop, Thomas A.; White, David L.; Jones, Steven M. Forest Ecology and Management, Vol. 47, Issue 1-4 https://doi.org/10.1016/0378-1127(92)90274-D	journal	January 1992
Projecting wildfire area burned in the south-eastern United States, 2011–60 Prestemon, Jeffrey P.; Shankar, Uma; Xiu, Aijun International Journal of Wildland Fire, Vol. 25, Issue 7 https://doi.org/10.1071/WF15124	journal	January 2016
Barcoded NS31/AML2 Primers for Sequencing of Arbuscular Mycorrhizal Communities in Environmental Samples Morgan, Benjamin S. T.; Egerton-Warburton, Louise M. Applications in Plant Sciences, Vol. 5, Issue 8 https://doi.org/10.3732/apps.1700017	journal	August 2017
Quantifying human impact on Earth's microbiome Pointing, Stephen B.; Fierer, Noah; Smith, Gavin J. D. Nature Microbiology, Vol. 1, Issue 9 https://doi.org/10.1038/nmicrobiol.2016.145	journal	August 2016
Arbuscular mycorrhizal fungal communities show low resistance and high resilience to wildfire disturbance Xiang, Xingjia; Gibbons, Sean M.; Yang, Jian Plant and Soil, Vol. 397, Issue 1-2 https://doi.org/10.1007/s11104-015-2633-z	journal	August 2015
Disturbance changes arbuscular mycorrhizal fungal phenology and soil glomalin concentrations but not fungal spore composition in montane rainforests in Veracruz and Chiapas, Mexico Violi, Helen A.; Barrientos-Priego, Alejandro F.; Wright, Sara F. Forest Ecology and Management, Vol. 254, Issue 2 https://doi.org/10.1016/j.foreco.2007.08.016	journal	January 2008
Deep Ion Torrent sequencing identifies soil fungal community shifts after frequent prescribed fires in a southeastern US forest ecosystem Brown, Shawn P.; Callaham, Mac A.; Oliver, Alena K. FEMS Microbiology Ecology, Vol. 86, Issue 3 https://doi.org/10.1111/1574-6941.12181	journal	August 2013
Context dependent fungal and bacterial soil community shifts in response to recent wildfires in the Southern Appalachian Mountains Brown, Shawn P.; Veach, Allison M.; Horton, Jonathan L. Forest Ecology and Management, Vol. 451 https://doi.org/10.1016/j.foreco.2019.117520	journal	November 2019
Spectrophotometric Determination of Nitrate with a Single Reagent Doane, Timothy A.; Horwáth, William R. Analytical Letters, Vol. 36, Issue 12 https://doi.org/10.1081/AL-120024647	journal	January 2003
A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi McGONIGLE, T. P.; Miller, M. H.; Evans, D. G. New Phytologist, Vol. 115, Issue 3 https://doi.org/10.1111/j.1469-8137.1990.tb00476.x	journal	July 1990
The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota) Öpik, M.; Vanatoa, A.; Vanatoa, E. New Phytologist, Vol. 188, Issue 1 https://doi.org/10.1111/j.1469-8137.2010.03334.x	journal	June 2010
Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand-replacing wildfire Baar, J.; Horton, T. R.; Kretzer, A. M. New Phytologist, Vol. 143, Issue 2 https://doi.org/10.1046/j.1469-8137.1999.00452.x	journal	August 1999
Plant functional groups associate with distinct arbuscular mycorrhizal fungal communities Davison, John; García de León, David; Zobel, Martin New Phytologist, Vol. 226, Issue 4 https://doi.org/10.1111/nph.16423	journal	February 2020
Urban mycorrhizas: predicting arbuscular mycorrhizal abundance in green roofs Chaudhary, V. Bala; Sandall, Emily L.; Lazarski, Martha V. Fungal Ecology, Vol. 40 https://doi.org/10.1016/j.funeco.2018.03.002	journal	August 2019
454-sequencing reveals stochastic local reassembly and high disturbance tolerance within arbuscular mycorrhizal fungal communities: Reassembly of AM fungal communities following disturbance Lekberg, Ylva; Schnoor, Tim; Kjøller, Rasmus Journal of Ecology, Vol. 100, Issue 1 https://doi.org/10.1111/j.1365-2745.2011.01894.x	journal	September 2011
VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R Chen, Hanbo; Boutros, Paul C. BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-35	journal	January 2011
Land‐use intensity and host plant identity interactively shape communities of arbuscular mycorrhizal fungi in roots of grassland plants Vályi, Kriszta; Rillig, Matthias C.; Hempel, Stefan New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13236	journal	December 2014
Urbanization erodes ectomycorrhizal fungal diversity and may cause microbial communities to converge Epp Schmidt, Dietrich J.; Pouyat, Richard; Szlavecz, Katalin Nature Ecology & Evolution, Vol. 1, Issue 5 https://doi.org/10.1038/s41559-017-0123	journal	April 2017
Ectomycorrhizal fungal spore bank recovery after a severe forest fire: some like it hot Glassman, Sydney I.; Levine, Carrie R.; DiRocco, Angela M. The ISME Journal, Vol. 10, Issue 5 https://doi.org/10.1038/ismej.2015.182	journal	October 2015
Effect of forest fire on number, viability and post-fire re-establishment of arbuscular mycorrhizae Rashid, A.; Ahmed, T.; Ayub, N. Mycorrhiza, Vol. 7, Issue 4 https://doi.org/10.1007/s005720050183	journal	November 1997
The phosphorus-rich signature of fire in the soil-plant system: a global meta-analysis Butler, Orpheus M.; Elser, James J.; Lewis, Tom Ecology Letters, Vol. 21, Issue 3 https://doi.org/10.1111/ele.12896	journal	January 2018
Effects of fire on arbuscular mycorrhizal fungi in the Mountain Chaco Forest Longo, Silvana; Nouhra, Eduardo; Goto, Bruno T. Forest Ecology and Management, Vol. 315 https://doi.org/10.1016/j.foreco.2013.12.027	journal	March 2014
Fire-severity effects on plant–fungal interactions after a novel tundra wildfire disturbance: implications for arctic shrub and tree migration Hewitt, Rebecca E.; Hollingsworth, Teresa N.; Stuart Chapin III, F. BMC Ecology, Vol. 16, Issue 1 https://doi.org/10.1186/s12898-016-0075-y	journal	May 2016
Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks Averill, Colin; Dietze, Michael C.; Bhatnagar, Jennifer M. Global Change Biology, Vol. 24, Issue 10 https://doi.org/10.1111/gcb.14368	journal	July 2018
Where are they hiding? Testing the body snatchers hypothesis in pyrophilous fungi Raudabaugh, Daniel B.; Matheny, P. Brandon; Hughes, Karen W. Fungal Ecology, Vol. 43 https://doi.org/10.1016/j.funeco.2019.100870	journal	February 2020
Mycorrhizal Fungi Can Dominate Phosphate Supply to Plants Irrespective of Growth Responses Smith, Sally E.; Smith, F. Andrew; Jakobsen, Iver Plant Physiology, Vol. 133, Issue 1 https://doi.org/10.1104/pp.103.024380	journal	September 2003
Climate Change and Forest Disturbances Dale, Virginia H.; Joyce, Linda A.; Mcnulty, Steve BioScience, Vol. 51, Issue 9 https://doi.org/10.1641/0006-3568(2001)051[0723:CCAFD]2.0.CO;2	journal	January 2001
Rapid, Sensitive, Microscale Determination of Phosphate in Water and Soil D'Angelo, Elisa; Crutchfield, J.; Vandiviere, M. Journal of Environmental Quality, Vol. 30, Issue 6 https://doi.org/10.2134/jeq2001.2206	journal	November 2001
Forest Fires and Climate Change in the 21ST Century Flannigan, M. D.; Amiro, B. D.; Logan, K. A. Mitigation and Adaptation Strategies for Global Change, Vol. 11, Issue 4 https://doi.org/10.1007/s11027-005-9020-7	journal	July 2006
Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales: Tansley review Johnson, Nancy Collins New Phytologist, Vol. 185, Issue 3 https://doi.org/10.1111/j.1469-8137.2009.03110.x	journal	December 2009
Fire as an evolutionary pressure shaping plant traits Keeley, Jon E.; Pausas, Juli G.; Rundel, Philip W. Trends in Plant Science, Vol. 16, Issue 8 https://doi.org/10.1016/j.tplants.2011.04.002	journal	August 2011
Frequent fire slows microbial decomposition of newly deposited fine fuels in a pyrophilic ecosystem Hopkins, Jacob R.; Huffman, Jean M.; Platt, William J. Oecologia, Vol. 193, Issue 3 https://doi.org/10.1007/s00442-020-04699-5	journal	July 2020
The Wildland–Urban Interface in the United States Radeloff, V. C.; Hammer, R. B.; Stewart, S. I. Ecological Applications, Vol. 15, Issue 3 https://doi.org/10.1890/04-1413	journal	June 2005
Duration and intensity of shade differentially affects mycorrhizal growth- and phosphorus uptake responses of Medicago truncatula KonvalinkovÃ¡, Tereza; PÃ¼schel, David; JanouÅ¡kovÃ¡, Martina Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00065	journal	February 2015
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Demographic controls of future global fire risk Knorr, W.; Arneth, A.; Jiang, L. Nature Climate Change, Vol. 6, Issue 8 https://doi.org/10.1038/nclimate2999	journal	May 2016
Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis Rúa, Megan A.; Antoninka, Anita; Antunes, Pedro M. BMC Evolutionary Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12862-016-0698-9	journal	June 2016
Anthropogenic land use shapes the composition and phylogenetic structure of soil arbuscular mycorrhizal fungal communities Moora, Mari; Davison, John; Öpik, Maarja FEMS Microbiology Ecology, Vol. 90, Issue 3 https://doi.org/10.1111/1574-6941.12420	journal	September 2014
Relationships Among Fires, Fungi, and soil Dynamics in Alaskan Boreal Forests Treseder, Kathleen K.; Mack, Michelle C.; Cross, Alison Ecological Applications, Vol. 14, Issue 6 https://doi.org/10.1890/03-5133	journal	December 2004
Forests and Climate Change: Forcings, Feedbacks, and the Climate Benefits of Forests Bonan, G. B. Science, Vol. 320, Issue 5882 https://doi.org/10.1126/science.1155121	journal	June 2008
Secret lifestyles of pyrophilous fungi in the genus Sphaerosporella Hughes, Karen W.; Case, Alexis; Matheny, P. Brandon American Journal of Botany, Vol. 107, Issue 6 https://doi.org/10.1002/ajb2.1482	journal	June 2020
More bang for the buck? Can arbuscular mycorrhizal fungal communities be characterized adequately alongside other fungi using general fungal primers? Lekberg, Ylva; Vasar, Martti; Bullington, Lorinda S. New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15035	journal	February 2018
Global diversity and distribution of arbuscular mycorrhizal fungi Kivlin, Stephanie N.; Hawkes, Christine V.; Treseder, Kathleen K. Soil Biology and Biochemistry, Vol. 43, Issue 11 https://doi.org/10.1016/j.soilbio.2011.07.012	journal	November 2011
Loss-on-Ignition as an Estimate of Soil Organic Matter Davies, Brian E. Soil Science Society of America Journal, Vol. 38, Issue 1 https://doi.org/10.2136/sssaj1974.03615995003800010046x	journal	January 1974
A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi Hoeksema, Jason D.; Chaudhary, V. Bala; Gehring, Catherine A. Ecology Letters, Vol. 13, Issue 3 https://doi.org/10.1111/j.1461-0248.2009.01430.x	journal	March 2010
FungalRoot: global online database of plant mycorrhizal associations Soudzilovskaia, Nadejda A.; Vaessen, Stijn; Barcelo, Milagros New Phytologist, Vol. 227, Issue 3 https://doi.org/10.1111/nph.16569	journal	May 2020
The wildland–urban interface dynamics in the southeastern U.S. from 1990 to 2000 Zhang, Yangjian; He, Hong S.; Yang, Jian Landscape and Urban Planning, Vol. 85, Issue 3-4 https://doi.org/10.1016/j.landurbplan.2007.11.007	journal	April 2008
Mycorrhizal phenotypes and the Law of the Minimum Johnson, Nancy Collins; Wilson, Gail W. T.; Wilson, Jacqueline A. New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13172	journal	November 2014
Pyrophilous fungi detected after wildfires in the Great Smoky Mountains National Park expand known species ranges and biodiversity estimates Hughes, Karen W.; Matheny, P. Brandon; Miller, Andrew N. Mycologia, Vol. 112, Issue 4 https://doi.org/10.1080/00275514.2020.1740381	journal	June 2020
Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus Hawkes, Christine V.; Hartley, Iain P.; Ineson, Phil Global Change Biology, Vol. 14, Issue 5 https://doi.org/10.1111/j.1365-2486.2007.01535.x	journal	May 2008

Similar Records

Woodland wildfire enables fungal colonization of encroaching Douglas‐fir

Journal Article · Thu Jun 08 00:00:00 EDT 2023 · Functional Ecology · OSTI ID:1840197

Smith, Gabriel Reuben; Peay, Kabir G.

Does the presence of large down wood at the time of a forest fire impact soil recovery?

Journal Article · Thu Feb 23 00:00:00 EST 2017 · Forest Ecology and Management · OSTI ID:1840197

Smith, Jane E.; Kluber, Laurel A.; Jennings, Tara N.; +3 more

Trajectories of change in sagebrush steppe vegetation communities in relation to multiple wildfires

Journal Article · Sun Jul 01 00:00:00 EDT 2012 · Ecological Applications · OSTI ID:1840197

Davies, G M; Bakker, J D; Dettweiler-Robinson, E; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Wildfire
Soil biogeochemistry
Plant-fungal symbiosis
Burn severity
Mycorrhizal fungi

Title: Arbuscular mycorrhizal fungal response to fire and urbanization in the Great Smoky Mountains National Park

Citation Formats

References (60)

Similar Records

Related Subjects