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Biological Invasions

, Volume 21, Issue 10, pp 3085–3099 | Cite as

Fungal communities do not recover after removing invasive Alliaria petiolata (garlic mustard)

  • M. A. AnthonyEmail author
  • K. A. Stinson
  • A. N. Trautwig
  • E. Coates-Connor
  • S. D. Frey
Original Paper

Abstract

The negative impacts of non-native invasive plants on native plants has prompted intensive eradication efforts, but whether eradication can restore soil microbial communities that are also sensitive to invasion is generally not considered. Some invasive plants, like Alliaria petiolata (garlic mustard), specifically alter soils in ways that promote the invasion process. Garlic mustard disrupts mycorrhizas, increases fungal pathogen loads, and elevates soil nutrient availability and soil pH; thus, the fungal community and soil property responses to garlic mustard eradication may be key to restoring ecosystem function in invaded forests. We conducted a garlic mustard eradication experiment at eight temperate, deciduous forests. 1 and 3 years after initiating annual garlic mustard removal (hand pulling), we collected soil samples and characterized fungal community structure using DNA metabarcoding alongside a suite of edaphic properties. We found that fungal richness, the number of shared fungal species, fungal biomass, and the relative abundance of fungal guilds became less similar to invaded plots by year three of eradication and more similar to uninvaded reference plots. However, fungal community composition did not resemble uninvaded communities by the third year of eradication and remained comparable to invaded communities. Soil chemical and physical properties also remained similar to invaded conditions. Overall soil abiotic–biotic restoration was not observed after 3 years of garlic mustard removal. Garlic mustard eradications may therefore not achieve management goals until soil physical, chemical, and biological properties become more similar to uninvaded forested areas or at least more dissimilar to invaded conditions that can promote invasion.

Keywords

Alliaria petiolata Fungi Garlic mustard Invasive species Mycorrhizal fungi Mycorrhizal symbiosis Restoration 

Notes

Acknowledgements

We thank Mel Knorr, Amber Kittle, and Christina Lyons for laboratory assistance. We thank Dustin Haines for field support. Sequencing was performed by James Ford and David Miller at the Center for Genomics and Bioinformatics at Indiana University. This work was funded by a U.S. Department of Defense Strategic Environmental Research and Development Program (SERDP) Grant (NRC2326) to KAS and SDF. Views, opinions, and/or findings contained in this report are those of the authors and should not be construed as an official Department of Defense position or decision unless so designated by other official documentation. MAA was supported by a National Science Foundation Graduate Research Fellowship (DGE 1450271).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2019_2031_MOESM1_ESM.docx (124 kb)
Supplementary material 1 (DOCX 124 kb)

References

  1. Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11:107–114CrossRefGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  3. Anderson RC, Kelley TM (1995) Growth of garlic mustard (Alliaria petiolata) in native soils of different acidity. Trans Ill State Acad Sci 88:91–96Google Scholar
  4. Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693CrossRefPubMedGoogle Scholar
  5. Anthony M, Frey S, Stinson K (2017) Fungal community homogenization, shift in dominant trophic guild, and appearance of novel taxa with biotic invasion. Ecosphere 8(9):e01951Google Scholar
  6. Bässler C, Heilmann-Clausen J, Karasch P, Brandl R, Halbwachs H (2015) Ectomycorrhizal fungi have larger fruiting bodies than saprotrophic fungi. Fungal Ecology 17:205–212CrossRefGoogle Scholar
  7. Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, De Wit P, Sánchez-García M, Ebersberger I, de Sousa F (2013) Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol 4:914–919Google Scholar
  8. Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184CrossRefPubMedGoogle Scholar
  9. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120.  https://doi.org/10.1093/bioinformatics/btu170 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bradshaw AD (1996) Underlying principles of restoration. Can J Fish Aquat Sci 53:3–9CrossRefGoogle Scholar
  11. Bradshaw AD, Chadwick MJ (1980) The restoration of land: the ecology and reclamation of derelict and degraded land. University of California Press, CaliforniaGoogle Scholar
  12. Braman RS, Hendrix SA (2002) Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium(III) reduction with chemiluminescence detection. Anal Chem 61(24):2715–2718CrossRefGoogle Scholar
  13. Burke DJ, Weintraub MN, Hewins CR, Kalisz S (2011) Relationship between soil enzyme activities, nutrient cycling and soil fungal communities in a northern hardwood forest. Soil Biol Biochem 43:795–803CrossRefGoogle Scholar
  14. Campbell R (1985) Longevity of Olpidium brassicae in air-dry soil and the persistence of the lettuce big-vein agent. Can J Bot 63:2288–2289CrossRefGoogle Scholar
  15. Caruso T, Hempel S, Powell J, Barto E, Rillig M (2012) Compositional divergence and convergence in arbuscular mycorrhizal fungal communities. Ecology 93:1115–1124CrossRefPubMedGoogle Scholar
  16. Castellano SM, Gorchov DL (2012) Reduced ectomycorrhizae on oak near invasive garlic mustard. Northeast Nat 19:1–24CrossRefGoogle Scholar
  17. Chao A, Ma K, Hsieh T, Chiu C (2016) SpadeR (species-richness prediction and diversity estimation in R): an R package in CRAN. Program and User’s Guide also published at http://chao.stat.nthu.edu.tw/wordpress/software_download
  18. Corbin JD, D’antonio CM (2012) Gone but not forgotten? Invasive plants’ legacies on community and ecosystem properties. Invasive Plant Sci Manag 5:117–124CrossRefGoogle Scholar
  19. Core R Team (2013) R development core team. RA Lang Environ Stat Comput 55:275–286Google Scholar
  20. Davison J, Moora M, Opik M, Adholeya A, Ainsaar L, Ba A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Ndiaye C, Partel M, Reier U, Saks U, Singh R, Vasar M, Zobel M (2015) FUNGAL SYMBIONTS. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973.  https://doi.org/10.1126/science.aab1161 CrossRefPubMedGoogle Scholar
  21. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461.  https://doi.org/10.1093/bioinformatics/btq461 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  23. Elgersma KJ, Ehrenfeld JG, Yu S, Vor T (2011) Legacy effects overwhelm the short-term effects of exotic plant invasion and restoration on soil microbial community structure, enzyme activities, and nitrogen cycling. Oecologia 167:733–745CrossRefPubMedGoogle Scholar
  24. Fernandez CW, Koide RT (2013) The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress. Fungal Ecol 6:479–486CrossRefGoogle Scholar
  25. Floudas D, Binder M, RileyR Barry K, Blanchette RA, Hrnrissat B, Martinez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719CrossRefPubMedGoogle Scholar
  26. Glassman SI, Wang IJ, Bruns TD (2017) Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales. Mol Ecol 26:6960–6973CrossRefPubMedGoogle Scholar
  27. Grove S, Haubensak KA, Parker IM (2012) Direct and indirect effects of allelopathy in the soil legacy of an exotic plant invasion. Plant Ecol 213:1869–1882CrossRefGoogle Scholar
  28. Güler P, Türkoglu A (2015) Screening of spore ornamentation of some mushrooms. J Biol Chem 43:119–125Google Scholar
  29. Halbwachs H, Brandl R, Bässler C (2015) Spore wall traits of ectomycorrhizal and saprotrophic agarics may mirror their distinct lifestyles. Fungal Ecol 17:197–204CrossRefGoogle Scholar
  30. Hartwright LM, Hunter PJ, Walsh JA (2010) A comparison of Olpidium isolates from a range of host plants using internal transcribed spacer sequence analysis and host range studies. Fungal Biol 114:26–33CrossRefPubMedGoogle Scholar
  31. Heilmann-Clausen J, Barron ES, Boddy L, Dahlberg A, Griffith GW, Nordén J, Ovaskainen O, Perini C, Senn-Irlet B, Halme P (2015) A fungal perspective on conservation biology. Conserv Biol 29:61–68CrossRefPubMedGoogle Scholar
  32. Ihrmark K, Bödeker IT, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandström-Durling M, Clemmensen KE (2012) New primers to amplify the fungal ITS2 region–evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol 82:666–677CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kiehl K, Kirmer A, Donath TW, Rasran L, Hölzel N (2010) Species introduction in restoration projects–evaluation of different techniques for the establishment of semi-natural grasslands in Central and Northwestern Europe. Basic Appl Ecol 11:285–299CrossRefGoogle Scholar
  34. Kivlin SN, Winston GC, Goulden ML, Treseder KK (2014) Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecol 12:14–25CrossRefGoogle Scholar
  35. Lankau RA (2011) Resistance and recovery of soil microbial communities in the face of Alliaria petiolata invasions. New Phytol 189:536–548CrossRefPubMedGoogle Scholar
  36. Lankau RA, Bauer JT, Anderson MR, Anderson RC (2014) Long-term legacies and partial recovery of mycorrhizal communities after invasive plant removal. Biol Invasions 16:1979–1990CrossRefGoogle Scholar
  37. Looney BP, Meidl P, Piatek MJ, Miettinen O, Martin FM, Matheny PB, Labbé JL (2018) Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates. New Phytol 218:54–65CrossRefPubMedGoogle Scholar
  38. Louca S, Polz MF, Mazel F, Albright MB, Huber JA, O’Connor MI, Ackermann M, Hahn AS, Srivastava DS, Crowe SA (2018) Function and functional redundancy in microbial systems. Nat Ecol Evol 2:936–943CrossRefPubMedGoogle Scholar
  39. Martiny JB, Martiny AC, Weihe C, Lu Y, Berlemont R, Brodie EL, Goulden ML, Treseder KK, Allison SD (2017) Microbial legacies alter decomposition in response to simulated global change. ISME J 11:490CrossRefPubMedGoogle Scholar
  40. Meekins JF, McCarthy BC (2000) Responses of the biennial forest herb Alliaria petiolata to variation in population density, nutrient addition and light availability. J Ecol 88:447–463CrossRefGoogle Scholar
  41. Mincheva T, Barni E, Varese G, Brusa G, Cerabolini B, Siniscalco C (2014) Litter quality, decomposition rates and saprotrophic mycoflora in Fallopia japonica (Houtt.) Ronse Decraene and in adjacent native grassland vegetation. Acta Oecol 54:29–35CrossRefGoogle Scholar
  42. Moeller HV, Peay KG, Fukami T (2014) Ectomycorrhizal fungal traits reflect environmental conditions along a coastal California edaphic gradient. FEMS Microbiol Ecol 87:797–806CrossRefPubMedGoogle Scholar
  43. 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 20:241–248CrossRefGoogle Scholar
  44. Northeast Regional Climate Center (2018) CLIMOD2. http://climod2.nrcc.cornell.edu. Accessed Feb 2019
  45. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Package ‘vegan’. Community ecology package, version 2(9)Google Scholar
  46. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefPubMedGoogle Scholar
  47. Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21:4122–4136CrossRefPubMedGoogle Scholar
  48. Pimental D (2007) Environmental and economic costs of vertebrate species invasions into the United States. Manag Vertebr Invasive Species 38:1–8Google Scholar
  49. Pinheiro J, Bates D, DebRoy S, Sarkar D (2007) Linear and nonlinear mixed effects models. R package version 3:57Google Scholar
  50. Prach K, Pyšek P (2001) Using spontaneous succession for restoration of human-disturbed habitats: experience from Central Europe. Ecol Eng 17:55–62CrossRefGoogle Scholar
  51. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715CrossRefGoogle Scholar
  52. Pyšek P, Richardson DM (2010) Invasive species, environmental change and management, and health. Annu Rev Environ Resour 35:25–55CrossRefGoogle Scholar
  53. Reid AM, Morin L, Downey PO, French K, Virtue JG (2009) Does invasive plant management aid the restoration of natural ecosystes? Biol Conserv 142:2342–2349CrossRefGoogle Scholar
  54. Rejmánek M, Pitcairn M (2002) When is eradication of exotic pest plants a realistic goal. Turning the tide: the eradication of invasive species, 249–253Google Scholar
  55. Ries L, Fletcher RJ Jr, Battin J, Sisk TD (2004) Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu Rev Ecol Evol Syst 35:491–522CrossRefGoogle Scholar
  56. Rodgers VL, Stinson KA, Finzi AC (2008) Ready or not, garlic mustard is moving in: Alliaria petiolata as a member of eastern North American forests. Bioscience 58:426–436CrossRefGoogle Scholar
  57. Simberloff D (2009) We can eliminate invasions or live with them. Successful management projects. Biol Invasions 11:149–157CrossRefGoogle Scholar
  58. Stanturf JA, Palik BJ, Williams MI, Dumroese RK, Madsen P (2014) Forest restoration paradigms. J Sustain For 33:S161–S194CrossRefGoogle Scholar
  59. Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:e140CrossRefPubMedPubMedCentralGoogle Scholar
  60. Stinson K, Kaufman S, Durbin L, Lowenstein F (2007) Impacts of garlic mustard invasion on a forest understory community. Northeast Nat 14:73–88CrossRefGoogle Scholar
  61. Stinson K, Frey SD, Jackson MR, Coates-Connr E, Anthony MA, Martinez K (2018) Responses of non-native earthworms to experimental eradication of garlic mustard and implications for native vegetation. Ecosphere 9:e02353CrossRefGoogle Scholar
  62. Tamura M, Tharayil N (2014) Plant litter chemistry and microbial priming regulate the accrual, composition and stability of soil carbon in invaded ecosystes. New Phytol 203:110–124CrossRefPubMedGoogle Scholar
  63. Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R, Villarreal Ruiz L, Vasco-Palacios AM, Thu PQ, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch K, Poldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Partel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson RH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson KH, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo LD, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, De Kesel A, Dang T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K (2014) Fungal biogeography: global diversity and geography of soil fungi. Science 346:1256688.  https://doi.org/10.1126/science.1256688 CrossRefPubMedGoogle Scholar
  64. Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci USA 101:10854–10861.  https://doi.org/10.1073/pnas.0403458101 CrossRefPubMedGoogle Scholar
  65. Török P, Helm A, Kiehl K, Buisoon E, Valkó O (2018) Beyond the species pool: modification of species dispersal, establishment, and assembly by habitat restoration. Restor Ecol 26:65–72CrossRefGoogle Scholar
  66. Twieg BD, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol 176:437–447CrossRefPubMedGoogle Scholar
  67. USDA NRCS National Plant Data Team (2018) Plant profile for Alliaria petiolata (garlic mustard). https://plants.usda.gov/core/profile?symbol=alpe4. Accessed Dec 2018
  68. Webster J, Weber R (2007) Introduction to fungi. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  69. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc: Guide Methods Appl 18:315–322Google Scholar
  70. Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States assessing the relative importance of habitat destruction, alien species, pollution, overexploitation, and disease. Bioscience 48:607–615CrossRefGoogle Scholar
  71. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Natural Resources and the EnvironmentUniversity of New HampshireDurhamUSA
  2. 2.Department of Environmental ConservationUniversity of MassachusettsAmherstUSA

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