Global pine tree invasions are linked to invasive root symbionts

Policelli, Nahuel; Hoeksema, Jason D.; Moyano, Jaime; Vilgalys, Rytas; Vivelo, Sasha; Bhatnagar, Jennifer M.

doi:10.1111/nph.18527

Global pine tree invasions are linked to invasive root symbionts

Journal Article · Tue Oct 11 00:00:00 UTC 2022 · New Phytologist

DOI:https://doi.org/10.1111/nph.18527· OSTI ID:2421601

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Boston Univ., MA (United States); OSTI
Univ. of Mississippi, Oxford, MS (United States)
Universidad Nacional del Comahue, San Carlos de Bariloche (Argentina)
Duke Univ., Durham, NC (United States)
Boston Univ., MA (United States)

Symbiotic soil microbes can facilitate plant invasions, yet it is unclear whether the invasive capacity of plants can be explained by the invasiveness of their microbial symbionts. After compiling a global dataset on associations between non-native invasive pine trees and ectomycorrhizal fungi (EMF), here we found that the interaction with invasive EMF is an important predictor of pine invasion success that acts in concert with aboveground plant traits, questioning the way we currently predict plant invasions.

View Accepted Manuscript (DOE)

Research Organization:: Boston Univ., MA (United States); Boston University, MA (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0020403

OSTI ID:: 2421601

Alternate ID(s):: OSTI ID: 1902438
OSTI ID: 2570218

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 1 Vol. 237; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (55)

Pinus contortainvasions increase wildfire fuel loads and may create a positive feedback with fire Taylor, Kimberley T.; Maxwell, Bruce D.; McWethy, David B. Ecology, Vol. 98, Issue 3 https://doi.org/10.1002/ecy.1673	journal	February 2017
Highly invasive tree species are more dependent on mutualisms Moyano, Jaime; Rodriguez‐Cabal, Mariano A.; Nuñez, Martin A. Ecology, Vol. 101, Issue 5 https://doi.org/10.1002/ecy.2997	journal	March 2020
Invasive trees rely more on mycorrhizas, countering the ideal‐weed hypothesis Moyano, Jaime; Rodriguez‐Cabal, Mariano A.; Nuñez, Martin A. Ecology, Vol. 102, Issue 5 https://doi.org/10.1002/ecy.3330	journal	April 2021
Spore Dispersal in Ectomycorrhizal Fungi at Fine and Regional Scales Horton, Thomas R. Biogeography of Mycorrhizal Symbiosis https://doi.org/10.1007/978-3-319-56363-3_3	book	January 2017
Non-native Pines Are Homogenizing the Ecosystems of South America García, Rafael A.; Franzese, Jorgelina; Policelli, Nahuel From Biocultural Homogenization to Biocultural Conservation https://doi.org/10.1007/978-3-319-99513-7_15	book	January 2018
Identities and distributions of the co-invading ectomycorrhizal fungal symbionts of exotic pines in the Hawaiian Islands Hynson, Nicole A.; Merckx, Vincent S. F. T.; Perry, Brian A. Biological Invasions, Vol. 15, Issue 11 https://doi.org/10.1007/s10530-013-0458-3	journal	April 2013
Tree invasions: patterns, processes, challenges and opportunities Richardson, David M.; Hui, Cang; Nuñez, Martin A. Biological Invasions, Vol. 16, Issue 3 https://doi.org/10.1007/s10530-013-0606-9	journal	December 2013
Invasive belowground mutualists of woody plants Nuñez, Martin A.; Dickie, Ian A. Biological Invasions, Vol. 16, Issue 3 https://doi.org/10.1007/s10530-013-0612-y	journal	December 2013
Towards management of invasive ectomycorrhizal fungi Dickie, Ian A.; Nuñez, Martin A.; Pringle, Anne Biological Invasions, Vol. 18, Issue 12 https://doi.org/10.1007/s10530-016-1243-x	journal	August 2016
Pine invasion impacts on plant diversity in Patagonia: invader size and invaded habitat matter Franzese, Jorgelina; Urrutia, Jonathan; García, Rafael A. Biological Invasions, Vol. 19, Issue 3 https://doi.org/10.1007/s10530-016-1344-6	journal	December 2016
Ecology and management of invasive Pinaceae around the world: progress and challenges Nuñez, Martin A.; Chiuffo, Mariana C.; Torres, Agostina Biological Invasions, Vol. 19, Issue 11 https://doi.org/10.1007/s10530-017-1483-4	journal	June 2017
Native and non-native trees can find compatible mycorrhizal partners in each other’s dominated areas Policelli, Nahuel; Horton, Thomas R.; García, Rafael A. Plant and Soil, Vol. 454, Issue 1-2 https://doi.org/10.1007/s11104-020-04609-x	journal	August 2020
Invasion Frameworks: a Forest Pathogen Perspective Paap, Trudy; Wingfield, Michael J.; Burgess, Treena I. Current Forestry Reports, Vol. 8, Issue 1 https://doi.org/10.1007/s40725-021-00157-4	journal	February 2022
Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial and temporal zonation? Peay, Kabir G.; Kennedy, Peter G.; Bruns, Thomas D. Fungal Ecology, Vol. 4, Issue 3 https://doi.org/10.1016/j.funeco.2010.09.010	journal	June 2011
Co-invasive exotic pines and their ectomycorrhizal symbionts show capabilities for wide distance and altitudinal range expansion Urcelay, Carlos; Longo, Silvana; Geml, József Fungal Ecology, Vol. 25 https://doi.org/10.1016/j.funeco.2016.11.002	journal	February 2017
Do people care about pine invasions? Visitor perceptions and willingness to pay for pine control in a protected area Bravo-Vargas, Valentina; García, Rafael A.; Pizarro, J. Cristóbal Journal of Environmental Management, Vol. 229 https://doi.org/10.1016/j.jenvman.2018.07.018	journal	January 2019
A proposed unified framework for biological invasions Blackburn, Tim M.; Pyšek, Petr; Bacher, Sven Trends in Ecology & Evolution, Vol. 26, Issue 7 https://doi.org/10.1016/j.tree.2011.03.023	journal	July 2011
Impacts of biological invasions: what's what and the way forward Simberloff, Daniel; Martin, Jean-Louis; Genovesi, Piero Trends in Ecology & Evolution, Vol. 28, Issue 1 https://doi.org/10.1016/j.tree.2012.07.013	journal	January 2013
What are mycorrhizal traits? Chaudhary, V. Bala; Holland, E. Penelope; Charman-Anderson, Suw Trends in Ecology & Evolution, Vol. 37, Issue 7 https://doi.org/10.1016/j.tree.2022.04.003	journal	July 2022
Microbial ecology of biological invasions van der Putten, Wim H.; Klironomos, John N.; Wardle, David A. The ISME Journal, Vol. 1, Issue 1 https://doi.org/10.1038/ismej.2007.9	journal	May 2007
Microbial invasions in terrestrial ecosystems Thakur, Madhav P.; van der Putten, Wim H.; Cobben, Marleen M. P. Nature Reviews Microbiology, Vol. 17, Issue 10 https://doi.org/10.1038/s41579-019-0236-z	journal	July 2019
Herbivores and the success of exotic plants: a phylogenetically controlled experiment Agrawal, Anurag A.; Kotanen, Peter M. Ecology Letters, Vol. 6, Issue 8 https://doi.org/10.1046/j.1461-0248.2003.00498.x	journal	August 2003
Naturalization and invasion of alien plants: concepts and definitions Richardson, David M.; Pysek, Petr; Rejmanek, Marcel Diversity Distributions, Vol. 6, Issue 2 https://doi.org/10.1046/j.1472-4642.2000.00083.x	journal	March 2000
Differences in endophyte communities of introduced trees depend on the phylogenetic relatedness of the receiving forest Gundale, Michael J.; Almeida, Juan P.; Wallander, Håkan Journal of Ecology, Vol. 104, Issue 5 https://doi.org/10.1111/1365-2745.12595	journal	August 2016
Identifying the role of soil microbes in plant invasions Dawson, Wayne; Schrama, Maarten Journal of Ecology, Vol. 104, Issue 5 https://doi.org/10.1111/1365-2745.12619	journal	August 2016
Global effects of non‐native tree species on multiple ecosystem services Castro‐Díez, Pilar; Vaz, Ana Sofia; Silva, Joaquim S. Biological Reviews https://doi.org/10.1111/brv.12511	journal	April 2019
Fungal functional ecology: bringing a trait‐based approach to plant‐associated fungi Zanne, Amy E.; Abarenkov, Kessy; Afkhami, Michelle E. Biological Reviews, Vol. 95, Issue 2 https://doi.org/10.1111/brv.12570	journal	November 2019
Trees and shrubs as invasive alien species - 2013 update of the global database Rejmánek, Marcel; Richardson, David M. Diversity and Distributions, Vol. 19, Issue 8 https://doi.org/10.1111/ddi.12075	journal	April 2013
Testing the co-invasion hypothesis: ectomycorrhizal fungal communities onAlnus glutinosaandSalix fragilisin New Zealand Bogar, Laura M.; Dickie, Ian A.; Kennedy, Peter G. Diversity and Distributions, Vol. 21, Issue 3 https://doi.org/10.1111/ddi.12304	journal	January 2015
Naturalized distributions show that climatic disequilibrium is structured by niche size in pines (Pinus L.) Perret, Daniel L.; Leslie, Andrew B.; Sax, Dov F. Global Ecology and Biogeography, Vol. 28, Issue 4 https://doi.org/10.1111/geb.12862	journal	December 2018
Evolution of Genome size in Pines (Pinus) and its Life-History Correlates: Supertree Analyses Grotkopp, Eva; Rejmánek,, Marcel; Sanderson, Michael J. Evolution, Vol. 58, Issue 8 https://doi.org/10.1111/j.0014-3820.2004.tb00456.x	journal	August 2004
Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change Talbot, J. M.; Allison, S. D.; Treseder, K. K. Functional Ecology, Vol. 22, Issue 6 https://doi.org/10.1111/j.1365-2435.2008.01402.x	journal	December 2008
Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules: MEASURING MYCORRHIZAL FUNGAL DISPERSAL Peay, Kabir G.; Schubert, Max G.; Nguyen, Nhu H. Molecular Ecology, Vol. 21, Issue 16 https://doi.org/10.1111/j.1365-294X.2012.05666.x	journal	June 2012
Conifers as invasive aliens: a global survey and predictive framework Richardson, David M.; Rejmánek, Marcel Diversity and Distributions, Vol. 10, Issue 5-6 https://doi.org/10.1111/j.1366-9516.2004.00096.x	journal	September 2004
Spread and impact of introduced conifers in South America: Lessons from other southern hemisphere regions: SPREAD AND IMPACT OF INTRODUCED CONIFERS Simberloff, Daniel; NuÑEz, Martin A.; Ledgard, Nicholas J. Austral Ecology, Vol. 35, Issue 5 https://doi.org/10.1111/j.1442-9993.2009.02058.x	journal	October 2009
Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems: Invasive microbes Litchman, Elena Ecology Letters, Vol. 13, Issue 12 https://doi.org/10.1111/j.1461-0248.2010.01544.x	journal	November 2010
Ectomycorrhizal ecology under primary succession on coastal sand dunes: interactions involving Pinus contorta, suilloid fungi and deer Ashkannejhad, Sara; Horton, Thomas R. New Phytologist, Vol. 169, Issue 2 https://doi.org/10.1111/j.1469-8137.2005.01593.x	journal	November 2005
Soil biota and invasive plants Reinhart, Kurt O.; Callaway, Ragan M. New Phytologist, Vol. 170, Issue 3 https://doi.org/10.1111/j.1469-8137.2006.01715.x	journal	May 2006
Inoculum potential of Rhizopogon spores increases with time over the first 4 yr of a 99-yr spore burial experiment Bruns, Thomas D.; Peay, Kabir G.; Boynton, Primrose J. New Phytologist, Vol. 181, Issue 2 https://doi.org/10.1111/j.1469-8137.2008.02652.x	journal	October 2008
Global patterns of ectomycorrhizal introductions Vellinga, Else C.; Wolfe, Benjamin E.; Pringle, Anne New Phytologist, Vol. 181, Issue 4 https://doi.org/10.1111/j.1469-8137.2008.02728.x	journal	January 2009
Water sources and controls on water‐loss rates of epigeous ectomycorrhizal fungal sporocarps during summer drought Lilleskov, Erik A.; Bruns, Thomas D.; Dawson, Todd E. New Phytologist, Vol. 182, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.02775.x	journal	March 2009
Co-invasion by Pinus and its mycorrhizal fungi Dickie, Ian A.; Bolstridge, Nicola; Cooper, Jerry A. New Phytologist, Vol. 187, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03277.x	journal	April 2010
No globally consistent effect of ectomycorrhizal status on foliar traits Koele, Nina; Dickie, Ian A.; Oleksyn, Jacek New Phytologist, Vol. 196, Issue 3 https://doi.org/10.1111/j.1469-8137.2012.04297.x	journal	September 2012
What determines pine naturalization: species traits, climate suitability or forestry use? McGregor, Kirsty F.; Watt, Michael S.; Hulme, Philip E. Diversity and Distributions, Vol. 18, Issue 10 https://doi.org/10.1111/j.1472-4642.2012.00942.x	journal	July 2012
Ectomycorrhizal fungal communities coinvading with P inaceae host plants in A rgentina: G ringos bajo el bosque Hayward, Jeremy; Horton, Thomas R.; Nuñez, Martin A. New Phytologist, Vol. 208, Issue 2 https://doi.org/10.1111/nph.13453	journal	May 2015
Suilloid fungi as global drivers of pine invasions Policelli, Nahuel; Bruns, Thomas D.; Vilgalys, Rytas New Phytologist, Vol. 222, Issue 2 https://doi.org/10.1111/nph.15660	journal	January 2019
Exploring the role of ectomycorrhizal fungi in soil carbon dynamics Zak, Donald R.; Pellitier, Peter T.; Argiroff, WilliamA. New Phytologist, Vol. 223, Issue 1 https://doi.org/10.1111/nph.15679	journal	February 2019
Early successional ectomycorrhizal fungi are more likely to naturalize outside their native range than other ectomycorrhizal fungi Vlk, Lukáš; Tedersoo, Leho; Antl, Tomáš New Phytologist, Vol. 227, Issue 5 https://doi.org/10.1111/nph.16557	journal	April 2020
An Invasive Plant Paradox Rout, Marnie E.; Callaway, Ragan M. Science, Vol. 324, Issue 5928 https://doi.org/10.1126/science.1173651	journal	May 2009
Plants, Mycorrhizal Fungi, and Bacteria: A Network of Interactions Bonfante, Paola; Anca, Iulia-Andra Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073504	journal	October 2009
Exotic Mammals Disperse Exotic Fungi That Promote Invasion by Exotic Trees Nuñez, Martin A.; Hayward, Jeremy; Horton, Thomas R. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0066832	journal	June 2013
Lack of belowground mutualisms hinders Pinaceae invasions Nuñez, Martin A.; Horton, Thomas R.; Simberloff, Daniel Ecology, Vol. 90, Issue 9 https://doi.org/10.1890/08-2139.1	journal	September 2009
A single ectomycorrhizal fungal species can enable a Pinus invasion Hayward, Jeremy; Horton, Thomas R.; Pauchard, Aníbal Ecology, Vol. 96, Issue 5 https://doi.org/10.1890/14-1100.1	journal	May 2015
What Attributes Make Some Plant Species More Invasive? Rejmanek, Marcel; Richardson, David M. Ecology, Vol. 77, Issue 6 https://doi.org/10.2307/2265768	journal	September 1996
The interplay between propagule pressure, seed predation and ectomycorrhizal fungi in plant invasion Moyano, Jaime; Chiuffo, Mariana C.; Policelli, Nahuel NeoBiota, Vol. 42 https://doi.org/10.3897/neobiota.42.30978	journal	February 2019

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