Abstract
Purpose
Pinaceae (pine family) trees are native to the Northern Hemisphere and their invasion into the Southern Hemisphere is a growing problem threatening biological diversity. Pinaceae are ectomycorrhizal (ECM) and their invasions are facilitated by non-native and co-invasive ECM fungi. Nothofagaceae species (southern beeches) are dominant overstory trees across large swaths of the Southern Hemisphere and are the only widespread ECM trees native to southern South America (SSA). This observational study investigates the in situ impact of Pinaceae invasions upon native soil fungi associated with Nothofagaceae hosts in SSA.
Methods
We performed soil nutrient testing and metabarcode sequencing of fungi in the rhizosphere of Nothofagus antarctica and Nothofagus dombeyi invaded by Pinaceae trees to determine whether co-invasive fungi might impact native soil fungi. Sampling transects extended from invasions into adjacent Nothofagus stands without invasive Pinaceae.
Results
The fungal community composition of the Nothofagaceae rhizosphere was dominated by plant-associated Mortierellaceae OTUs in metabarcode data. Mortierellaceae OTU relative abundance was significantly reduced near invasions of Pinus contorta (Pinaceae). Invasions of Pseudotsuga menziesii (Pinaceae) and Pinus contorta were associated with reduced relative abundance of Nothofagus-associated ECM OTUS in the Nothofagus rhizosphere. Pinus contorta invasions were also associated with reduced soil organic matter, total carbon, total phosphorus, and total nitrogen.
Conclusion
Further empirical study is warranted to investigate the hypothesis that Mortierellaceae and Pinaceae-specific /suillus-rhizopogon ECM fungi compete for nutrients bound in soil organic matter. Such competition may have potential long-term legacy effects upon post-invasion restoration efforts and implications for Pinaceae invasions globally.
Similar content being viewed by others
Data availability
Genetic data: Raw sequence reads presented in this manuscript are deposited in the GenBank Short Read Archive (SRA) (BioProject number: PRJNA916756).
References
Abarenkov K, Tedersoo L, Nilsson RH, Vellak K, Saar I, Veldre V, … Kõljalg U (2010) PlutoF—a Web Based Workbench for Ecological and Taxonomic Research, with an Online Implementation for Fungal ITS Sequences. Evol Bioinform Online 6:189–196. https://doi.org/10.4137/EBO.S6271
Abuzinadah RA, Finlay RD, Read DJ (1986) The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. New Phytologist 103(3):495–506. https://doi.org/10.1111/j.1469-8137.1986.tb02887.x
Anderson MJ (2006) Distance-Based Tests for Homogeneity of Multivariate Dispersions. Biometrics 62(1):245–253
Ashkannejhad S, Horton TR (2006) Ectomycorrhizal ecology under primary succession on coastal sand dunes: interactions involving Pinus contorta, suilloid fungi and deer. New Phytol 169:345–354
Bahram M, Kõljalg U, Kohout P, Mirshahvaladi S, Tedersoo T (2013) Ectomycorrhizal fungi of exotic pine plantations in relation to native host trees in Iran: evidence of host range expansion by local symbionts to distantly related host taxa. Mycorrhiza 23(1):11–19. https://doi.org/10.1007/s00572-012-0445-z
Baohanta R, Thioulouse J, Ramanankierana H, Prin Y, Rasolomampianina R, Baudoin E, Rakotoarimanga N et al (2012) Restoring native forest ecosystems after exotic tree plantation in Madagascar: combination of the local ectotrophic species Leptolena bojeriana and Uapaca bojeri mitigates the negative influence of the exotic species Eucalyptus camaldulensis and Pinus patula. Biol Invasions 14(11):2407–2421. https://doi.org/10.1007/s10530-012-0238-5
Blanck YL, Gowda J, Mårtensson LM, Sandberg J, Fransson AM (2011) Plant species richness in a natural Argentinian matorral shrub-land correlates negatively with levels of plant phosphorus. Plant Soil 345(1–2):11–21. https://doi.org/10.1007/s11104-010-0671-0
Bonito G, Hameed K, Ventura R, Krishnan J, Schadt CW, Vilgalys R (2016) Isolating a functionally relevant guild of fungi from the root microbiome of Populus. Fungal Ecol 22:35–42. https://doi.org/10.1016/j.funeco.2016.04.007
Bremner JM (1965) Inorganic forms of nitrogen. In: Black CA, et al. Eds. Methods of soil analysis, Part 2. Chemical and Microbiological Properties. Agronomy Monograph No. 9, ASA and SSSA, Madison, 1179–1237
Bremner JM (1996) Nitrogen—Total. In: Sparks, D.L., et al. Eds. Methods of Soil Analysis. Part 3. Chemical Methods. SSSA Book Ser. 5. SSSA and ASA, Madison, WI. p. 1085–1089
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220(4):1108–1115. https://doi.org/10.1111/nph.14976
Bruns TD, Peay KG, Boynton PJ, Grubisha LC, Hynson NA, Nguyen NH, Rosenstock NP (2009) Inoculum potential of Rhizopogon spores increases with time over the first 4 yr of a 99-yr spore burial experiment. New Phytol 181(2):463–470. https://doi.org/10.1111/j.1469-8137.2008.02652.x
Budde KB, Gallo L, Marchelli P, Mosner E, Liepelt S, Ziegenhagen B, Leyer I (2011) Wide spread invasion without sexual reproduction? A case study on European willows in Patagonia, Argentina. Biol Invasions 13(1):45–54. https://doi.org/10.1007/s10530-010-9785-9
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, … Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303
Carron AI, Garibaldi LA, Marquez S, Fontenla S (2020) The soil fungal community of native woodland in Andean Patagonian forest: A case study considering experimental forest management and seasonal effects. For Ecol Manag 461:117955. https://doi.org/10.1016/j.foreco.2020.117955
Chapela IH, Osher LJ, Horton TR, Henn MR (2001) Ectomycorrhizal fungi introduced with exotic pine plantations induce soil carbon depletion. Soil Biol Biochem 33(12):1733–1740. https://doi.org/10.1016/S0038-0717(01)00098-0
Corrales A, Mangan SA, Turner BL, Dalling JW, Chave J (2016) An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecol Lett 19(4):383–392. https://doi.org/10.1111/ele.12570
Dehlin H, Peltzer DA, Allison VJ, Yeates GW, Nilsson MC, Wardle DA (2008) Tree Seedling Performance and below-ground properties in stands of invasive and native tree species. N Z J Ecol 32(1):67–79
Dickie IA, Bolstridge N, Cooper JA, Peltzer DA (2010) Co-invasion by Pinus and its mycorrhizal fungi. New Phytol 187(2):475–484. https://doi.org/10.1111/j.1469-8137.2010.03277.x
Dickie IA, St John MG, Yeates GW, Morse CW, Bonner KI, Orwin K, Peltzer DA (2014) Belowground legacies of Pinus contorta invasion and removal result in multiple mechanisms of invasional meltdown. AoB Plants 6(1):plu056. https://doi.org/10.1093/aobpla/plu05
Dickie IA, Bufford JL, Cobb RC, Desprez-Loustau M-L, Grelet G, Hulme PE, Klironomos J, Makiola A, Nuñez MA, Pringle A, Thrall PH, Tourtellot SG, Waller L, Williams NM (2017) The emerging science of linked plant-fungal invasions. New Phytol 215(4):1314–1332. https://doi.org/10.1111/nph.14657
Durall DM, Todd AW, Trappe JM (1994) Decomposition of 14C-labelled substrates by ectomycorrhizal fungi in association with Douglas fir. New Phytologist 127(4):725–729. https://doi.org/10.1111/j.1469-8137.1994.tb02976.x
Erlandson SR, Savage JA, Cavender-Bares JM, Peay KG (2016) Soil moisture and chemistry influence diversity of ectomycorrhizal fungal communities associating with willow along an hydrologic gradient. FEMS Microbiol Ecol 92(1). https://doi.org/10.1093/femsec/fiv148
Farjon A (2010) A Handbook of the World’s Conifers. BRILL, Leiden, Netherlands
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118
Gandolfo MA, Hermsen EJ, Zamaloa MC, Nixon KC, González CC, Wilf P, Cúneo NR, Johnson KR (2011) Oldest known Eucalyptus macrofossils are from South America. PLoS One 6(6). https://doi.org/10.1371/journal.pone.0021084
García RA, Franzese J, Policelli N, Sasal Y, Zenni RD, Nuñez MA, Taylor K, Pauchard A (2018) Non-native Pines Are Homogenizing the Ecosystems of South America. In Rozzi R, May Jr RH, Chapin III FS, Massardo F, Gavin MC, Klaver IJ, Pauchard A, Nuñez MA, Simberloff D (Eds.), From Biocultural Homogenization to Biocultural Conservation (pp. 245–263). Springer International Publishing. https://doi.org/10.1007/978-3-319-99513-7_15
Gehring CA, Swaty RL, Deckert RJ (2017) Chapter 16—Mycorrhizas, Drought, and Host-Plant Mortality. In Johnson NC et al. (Eds.) Mycorrhizal Mediation of Soil pp. 279–298. Elsevier. Amsterdam, Netherlands. https://doi.org/10.1016/B978-0-12-804312-7.00016-4
Gloor GB, Macklaim JM, Pawlowsky-Glahn V, Egozcue JJ (2017) Microbiome datasets are compositional: and this is not optional. Front Microbiol 8:2224. https://doi.org/10.3389/fmicb.2017.02224
Grove S, Haubensak KA, Gehring C, Parker IM (2017) Mycorrhizae, invasions, and the temporal dynamics of mutualism disruption. J Ecol 105(6):1496–1508. https://doi.org/10.1111/1365-2745.12853
Gut B (2008) Trees in Patagonia. Birkhäuser Verlag AG, Basel, Switzerland
Hayward J, Horton TR, Nuñez MA (2015a) Ectomycorrhizal fungal communities coinvading with Pinaceae host plants in Argentina: Gringos bajo el bosque. New Phytol 208(2):497–506. https://doi.org/10.1111/nph.13453
Hayward J, Horton TR, Pauchard A, Nuñez MA (2015b) A single ectomycorrhizal fungal species can enable a Pinus invasion. Ecology 96(5):1438–1444. https://doi.org/10.1890/14-1100.1
Heenan PB, Smissen RD (2013) Revised circumscription of Nothofagus and recognition of the segregate genera Fuscospora, Lophozonia, and Trisyngyne (Nothofagaceae). Phytotaxa 146(1):1–31. https://doi.org/10.11646/phytotaxa.146.1.1
Hill RS (2001) Biogeography, evolution and palaeoecology of Nothofagus (Nothofagaceae): the contribution of the fossil record. Aust J Bot 49:321–332
Hill RS, Beer YK, Hill KE, Maciunas E, Tarran MA, Wainman CC (2017) Evolution of the eucalypts – an interpretation from the macrofossil record. Aust J Bot 64(8):600–608. https://doi.org/10.1071/BT16117
Hermsen EJ, Gandolfo MA, Zamaloa MD (2012) The fossil record of Eucalyptus in patagonia. Am J Bot 99(8):1356–1374. https://doi.org/10.3732/ajb.1200025
Hoeksema JD, Averill C, Bhatnagar JM, Brzostek E, Buscardo E, Chen K-H, Liao H-L, Nagy L, Policelli N, Ridgeway J, Rojas JA, Vilgalys R (2020) Ectomycorrhizal Plant-Fungal Co-invasions as Natural Experiments for Connecting Plant and Fungal Traits to Their Ecosystem Consequences. Front For Glob Change 3:84. https://doi.org/10.3389/ffgc.2020.00084
Horak E (1983) Mycogeography in the south Pacific region: Agaricales, Boletales. Aust J Bot Suppl Ser 10:1–41
Johnson JM, Ludwig A, Furch ACU, Mithöfer A, Scholz S, Reichelt M, Oelmüller R (2018) The Beneficial Root-Colonizing Fungus Mortierella hyalina Promotes the Aerial Growth of Arabidopsis and Activates Calcium-Dependent Responses That Restrict Alternaria brassicae–Induced Disease Development in Roots. Mol Plant Microbe Interact 32(3):351–363. https://doi.org/10.1094/MPMI-05-18-0115-R
Kõljalg U, Larsson K-H, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Ursing BM (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166(3):1063–1068. https://doi.org/10.1111/j.1469-8137.2005.01376.x
Kuhar F, Smith ME, Mujic A, Truong C, Nouhra E (2017) A systematic overview of Descolea (Agaricales) in the Nothofagaceae forests of Patagonia. Fungal Biol 121(10):876–889. https://doi.org/10.1016/j.funbio.2017.06.006
Kuo S (1996) Phosphorus. In: Sparks DL, et al. (Eds) Methods of Soil Analysis. Part 3. Chemical Methods. SSSA Book Ser. 5. SSSA and ASA, Madison, WI 869–920
Langdon B, Pauchard A, Aguayo M (2010) Pinus contorta invasion in the Chilean Patagonia: Local patterns in a global context. Biol Invasions 12(12):3961–3971. https://doi.org/10.1007/s10530-010-9817-5
Liao H-L, Bonito G, Rojas JA, Hameed K, Wu S, Schadt CW, Labbé J, Tuskan GA, Martin F, Grigoriev IV, Vilgalys R (2019) Fungal Endophytes of Populus trichocarpa Alter Host Phenotype, Gene Expression, and Rhizobiome Composition. Mol Plant-Microbe Interact 32(7). https://doi.org/10.1094/MPMI-05-18-0133-R
Marchelli P, Pastorino MJ, Gallo LA (2021) Temperate subantarctic forests: A huge natural laboratory. In: Marchelli P, Pastorino M, Gallo L (eds) Low intensity breeding of native forest trees in Argentina. Springer, Cham, pp 27–54
McMurdie PJ, Holmes S (2013) phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS One 8(4):e61217. https://doi.org/10.1371/journal.pone.0061217
Nguyen NH, Hynson NA, Bruns TD (2012) Stayin’ alive: Survival of mycorrhizal fungal propagules from 6-yr-old forest soil. Fungal Ecol 5(6):741–746. https://doi.org/10.1016/j.funeco.2012.05.006
Nguyen NH, Smith D, Peay K, Kennedy P (2015) Parsing ecological signal from noise in next generation amplicon sequencing. New Phytol 205(4):1389–1393. https://doi.org/10.1111/nph.12923
Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
Ning C, Egerton-Warburton LM, Mueller GM, Xiang W, Yan W, Liu S (2021) Shifts in ectomycorrhizal fungal community composition during the early establishment of native and exotic pine seedlings. Appl Soil Ecol 157:103722. https://doi.org/10.1016/j.apsoil.2020.103722
Nouhra ER, Urcelay C, Longo MS, Fontenla S (2012) Differential hypogeous sporocarp production from Nothofagus dombeyi and N. pumilio forests in southern Argentina. Mycologia 104(1):45–52. https://doi.org/10.3852/11-098
Nouhra E, Urcelay C, Longo S, Tedersoo L (2013) Ectomycorrhizal fungal communities associated to Nothofagus species in Northern Patagonia. Mycorrhiza 23(6):487–496. https://doi.org/10.1007/s00572-013-0490-2
Nuñez MA, Hayward J, Horton TR, Amico GC, Dimarco RD, Barrios-Garcia MN, Simberloff D (2013) Exotic Mammals Disperse Exotic Fungi That Promote Invasion by Exotic Trees. PLoS One 8(6):e66832. https://doi.org/10.1371/journal.pone.0066832
Nuñez MA, Chiuffo MC, Torres A, Paul T, Dimarco RD, Raal P, Policelli N, Moyano J, García RA, van Wilgen BW, Pauchard A, Richardson DM (2017) Ecology and management of invasive Pinaceae around the world: progress and challenges. Biol Invasions 19(11):3099–3120. https://doi.org/10.1007/s10530-017-1483-4
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) vegan: Community Ecology Package. R package version 2.4–6. Retrieved November 11, 2022, from https://CRAN.R-project.org/package=vegan
Phillips LA, Ward V, Jones MD (2014) Ectomycorrhizal fungi contribute to soil organic matter cycling in sub-boreal forests. ISME J 8(3):699–713. https://doi.org/10.1038/ismej.2013.195
Plett JM, Daguerre Y, Wittulsky S, Vayssières A, Deveau A, Melton SJ, Kohler A, Morrell-Falvey JL, Brun A, Veneault-Fourrey C, Martin F (2014) Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. Proc Nat Acad Sci 111(22):8299–304. https://doi.org/10.1073/pnas.1322671111
Policelli N, Bruns TD, Vilgalys R, Nuñez MA (2019) Suilloid fungi as global drivers of pine invasions. New Phytol 222(2):714–725. https://doi.org/10.1111/nph.15660
Policelli N, Horton TR, García RA, Naour M, Pauchard A, Nuñez MA (2020) Native and non-native trees can find compatible mycorrhizal partners in each other’s dominated areas. Plant Soil 454(1):285–297. https://doi.org/10.1007/s11104-020-04609-x
Policelli N, Horton TR, Kitzberger T, Nuñez MA (2022a) Invasive ectomycorrhizal fungi can disperse in the absence of their known vectors. Fungal Ecol 55:101124. https://doi.org/10.1016/j.funeco.2021.101124
Policelli N, Vietorisz C, Bhatnagar JM, Nuñez MA (2022b) Ectomycorrhizal fungi invasions in Southern South America. In: Lugo MA, Pagano MC (eds) Mycorrhizal fungi in South America: biodiversity, conservation, and sustainable food production. Springer International Publishing, Cham, pp 25–46. https://doi.org/10.1007/978-3-031-12994-0_2
Policelli N, Hoeksema JD, Moyano J, Vilgalys R, Vivelo S, Bhatnagar JM (2022c) Global pine tree invasions are linked to invasive root symbionts. New Phytol 237(1):16–21. https://doi.org/10.1111/nph.18527
Reynolds NK, Jusino MA, Stajich JE, Smith ME (2022) Understudied, underrepresented, and unknown: Methodological biases that limit detection of early diverging fungi from environmental samples. Mol Ecol Resour 22(3):1065–1085. https://doi.org/10.1111/1755-0998.13540
Salomón MES, Barroetaveña C, Pildain MB, Williams EA, Rajchenberg M (2018) What happens to the mycorrhizal communities of native and exotic seedlings when Pseudotsuga menziesii invades Nothofagaceae forests in Patagonia, Argentina? Acta Oecol 91:108–119. https://doi.org/10.1016/j.actao.2018.07.003
Simberloff D, Relva MA, Nunez M (2003) Introduced species and management of a Nothofagus/Austrocedrus forest. Environ Manag 31(2):263–275. https://doi.org/10.1007/s00267-002-2794-4
Skrede I, Engh IB, Binder M, Carlsen T, Kauserud H, Bendiksby M (2011) Evolutionary history of Serpulaceae (Basidiomycota): molecular phylogeny, historical biogeography and evidence for a single transition of nutritional mode. BMC Evol Biol 11(1):1–13
Sukdeo N, Teen E, Rutherford PM, Massicotte HB, Egger KN (2019) Bacterial and fungal saprotrophs are strongly stimulated weeks to months after forest soil profile reconstruction. Pedobiologia 73:29–41. https://doi.org/10.1016/j.pedobi.2019.01.001
Thomas LK, Leyer I (2014) Age structure, growth performance and composition of native and invasive Salicaceae in Patagonia. Plant Ecol 215(9):1047–1056. https://doi.org/10.1007/s11258-014-0362-7
Thomas LK, Mosner E, Leyer I (2015) River dynamics and invasion: Distribution patterns of native and invasive woody vegetation at the Río Negro, Argentina. Riparian Ecol Conserv 2(1):45–57. https://doi.org/10.1515/remc-2015-0001
Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: Global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20(4):217–263. https://doi.org/10.1007/s00572-009-0274-x
Tedersoo L, Bahram M, Toots M, Diédhiou AG, Henkel TW, Kjøller R, Kõljalg U (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21(17):4160–4170. https://doi.org/10.1111/j.1365-294X.2012.05602.x
Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: Foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27(3):83–99. https://doi.org/10.1016/j.fbr.2013.09.001
Truong C, Mujic AB, Healy R, Kuhar F, Furci G, Torres D, Niskanen T, Sandoval‐Leiva PA, Fernández N, Escobar JM, Moretto A, Palfner G, Pfister D, Nouhra E, Swenie R, Sánchez‐García M, Matheny PB, Smith ME (2017) How to know the fungi: combining field inventories and DNA‐barcoding to document fungal diversity. New Phytologist 214(3):913–919. https://doi.org/10.1111/nph.14509
Truong C, Gabbarini LA, Corrales A, Mujic AB, Escobar JM, Moretto A, Smith ME (2019) Ectomycorrhizal fungi and soil enzymes exhibit contrasting patterns along elevation gradients in southern Patagonia. New Phytologist 222(4):1936–1950. https://doi.org/10.1111/nph.15714
Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, Al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, Boekhout T, Crous PW, Robert V, Verkley GJM (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Stud Mycol 92:135–154. https://doi.org/10.1016/j.simyco.2018.05.001
White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA et al (eds) PCR protocols: a guide to methods and applications. Academic Press, United States, pp 315–322
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Acknowledgements
The authors would like to thank Viviana Pangare and Jorge Greco of La Reserva El Foyel for their kind assistance and for permitting research access to the reserve. We would also like to thank Parques Nacionales de Argentina for issuing research and collection permits (projects 720, 1444, and 1543) and Dr. Eduardo Nouhra for his assistance in coordinating the permit for project 720.
Funding
This work was supported by National Science Foundation grant DEB 1354802 (M.E.S.) and an Advanced Postdoc Mobility Fellowship (P300P3_158523) from the Swiss National Science Foundation (C.T.).
Author information
Authors and Affiliations
Contributions
The Research was designed by Alija Bajro Mujic, Martin Nuñez, and Matthew Smith. Field locality selection and field collection was performed by Alija Bajro Mujic and Nahuel Policelli. All analyses were performed by Alija Bajro Mujic and Camille Truong. The manuscript was written by Alija Bajro Mujic with significant contributions from all co-authors.
Corresponding author
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Responsible Editor: Janusz J Zwiazek.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Mujic, A.B., Policelli, N., Nuñez, M.A. et al. Co-invasive ectomycorrhizal fungi alter native soil fungal communities. Plant Soil 484, 547–567 (2023). https://doi.org/10.1007/s11104-022-05820-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05820-8