Skip to main content
SpringerLink
Log in

Fungi from a non-native invasive plant increase its growth but have different growth effects on native plants

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Non-native invasive plants can associate with and accumulate microbes in their introduced range, which may transfer to native plants and potentially exert pathogenic effects. In these cases, the invasive plant can act as a pathogen reservoir. However, little is known about this as a possible plant invasion mechanism. We isolated fungi from the roots of 32 Vincetoxicum rossicum (Apocynaceae) plants collected across Ontario, Canada, where it is highly invasive. The growth effects of known pathogenic fungi were tested on V. rossicum and two commonly co-occurring native plants, Asclepias syriaca (Apocynaceae) and Solidago canadensis (Asteraceae). We hypothesised that these fungi would reduce the growth of native plants more than that of V. rossicum. Of the18 fungal taxa isolated from V. rossicum roots, 15 were previously reported as pathogens on other plants and 16 represent new records on this plant. Four of the seven fungi tested on V. rossicum increased its total biomass and/or root-shoot ratio compared to uninoculated controls. When inoculated individually, three of these fungi had neutral growth effects on the native plants. However, when inoculated together, Cadophora sp., Ilyonectria radicicola, and Macrophomina phaseolina reduced the total biomass of S. canadensis. These results support that at least in some cases non-native invaders may benefit from associating with soil microbes that can function as pathogens on native plants. These differential functional outcomes between non-native invasive and native plants may be important for mediating plant community structure and the persistence of invasive plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aegerter BJ, Gordon TR, Davis RM (2000) Occurrence and pathogenicity of fungi associated with melon root rot and vine decline in California. Plant Dis 84:224–230. doi:10.1094/PDIS.2000.84.3.224

    Article  Google Scholar 

  • Agrawal AA, Kotanen PM, Mitchell CE, Power AG, Godsoe W, Klironomos J (2005) Enemy release? An experiment with congeneric plant pairs and diverse above- and belowground enemies. Ecology 86:2979–2989. doi:10.1890/05-0219

    Article  Google Scholar 

  • Agrios GN (2005) Plant pathology, 5th edn. Elsevier, Burlington

    Google Scholar 

  • Anderson JM, Aitken EAB, Dann EK, Coates LM (2013) Morphological and molecular diversity of Colletotrichum spp. causing pepper spot and anthracnose of lychee (Litchi chinensis) in Australia. Plant Pathol 62:279–288. doi:10.1111/j.1365-3059.2012.02632.x

    Article  CAS  Google Scholar 

  • Andrade-Linares DR, Grosch R, Franken P, Rexer K-H, Kost G, Restrepo S, de Garcia MCC, Maximova E (2011) Colonization of roots of cultivated Solanum lycopersicum by dark septate and other ascomycetous endophytes. Mycologia 103:710–721. doi:10.3852/10-329

    Article  PubMed  Google Scholar 

  • Armengol J, Vicent A, Martínez-Culebras P, Bruton BD, García-Jiménez J (2003) Identification, occurrence and pathogenicity of Rhizopycnis vagum on muskmelon in Spain. Plant Pathol 52:68–73. doi:10.1046/j.1365-3059.2003.00796.x

    Article  Google Scholar 

  • Averill KM, DiTommaso A, Mohler CL, Milbrath LR (2010) Establishment of the invasive perennial Vincetoxicum rossicum across a disturbance gradient in New York State, USA. Plant Ecol 211:65–77. doi:10.1007/s11258-010-9773-2

    Article  Google Scholar 

  • Beckstead J, Meyer SE, Connolly BM, Huck MB, Street LE (2010) Cheatgrass facilitates spillover of a seed bank pathogen onto native grass species. J Ecol 98:168–177. doi:10.1111/j.1365-2745.2009.01599.x

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300

    Google Scholar 

  • Bent E (2006) Induced systemic resistance mediated by plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF). In: Tuzun S, Bent E (eds) Multigenic and induced systemic resistance in plants. Springer, New York, pp 225–258

    Chapter  Google Scholar 

  • Berner D, Cavin C, Mukhina Z, Kassanelly D (2011) Leaf anthracnose, a new disease of swallow-worts caused by Colletotrichum lineola from Russia. Plant Dis 95:1586. doi:10.1094/PDIS-04-11-0318

    Article  Google Scholar 

  • Bongard C, Butler K, Fulthorpe R (2013a) Investigation of fungal root colonizers of the invasive plant Vincetoxicum rossicum and co-occurring local native plants in a field and woodland area in Southern Ontario. Nat Conserv 4:55–76. doi:10.3897/natureconservation.4.3578

    Article  Google Scholar 

  • Bongard CL, Navaranjan G, Yan W, Fulthorpe RR (2013b) Fungal colonization of the invasive vine Vincetoxicum rossicum and native plants. Plant Ecol Evol 146:45–52. doi:10.5091/plecevo.2013.739

    Article  Google Scholar 

  • Cabral A, Rego C, Nascimento T, Oliveira H, Groenewald JZ, Crous PW (2012a) Multi-gene analysis and morphology reveal novel Ilyonectria species associated with black foot disease of grapevines. Fungal Biol 116:62–80. doi:10.1016/j.funbio.2011.09.010

    Article  PubMed  CAS  Google Scholar 

  • Cabral A, Groenewald JZ, Rego C, Oliveira H, Crous PW (2012b) Cylindrocarpon root rot: multi-gene analysis reveals novel species within the Ilyonectria radicicola species complex. Mycol Prog 11:655–688. doi:10.1007/s11557-011-0777-7

    Article  Google Scholar 

  • Canty A, Ripley BD (2014) boot: Bootstrap R (S-Plus) Functions. R package version 1.3-13

  • Cappuccino N (2004) Allee effect in an invasive alien plant, pale swallow-wort Vincetoxicum rossicum (Asclepiadaceae). Oikos 106:3–8. doi:10.1111/j.0030-1299.2004.12863.x

    Article  Google Scholar 

  • Cappuccino N, Mackay R, Eisner C (2002) Spread of the invasive alien vine Vincetoxicum rossicum: tradeoffs between seed dispersability and seed quality. Am Midl Nat 148:263–270. doi:10.1674/0003-0031(2002)148[0263:SOTIAV]2.0.CO;2

    Article  Google Scholar 

  • Carlucci A, Raimondo ML, Santos J, Phillips AJL (2012) Plectosphaerella species associated with root and collar rots of horticultural crops in southern Italy. Persoonia Mol Phylogeny Evol Fungi 28:34–48. doi:10.3767/003158512X638251

    Article  CAS  Google Scholar 

  • Causin R, Finozzi V, Montecchio L, Accordi Mutto S (2004) First report of Geniculosporium corticioides on Common Oak in Italy. J Plant Pathol 86:177

    Google Scholar 

  • Couture L, Brisson JD, Émond G (2003) Names of plant diseases in Canada, 4th edn. Québec Society for the Protection of Plants, Québec

    Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449. doi:10.1098/rstb.2012.0331

    Article  PubMed  CAS  Google Scholar 

  • Davison AC, Hinkley DV (1997) Bootstrap methods and their applications. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Day NJ, Dunfield KE, Antunes PM (2015) Temporal dynamics of plant–soil feedback and root-associated fungal communities over 100 years of invasion by a non-native plant. J Ecol. doi:10.1111/1365-2745.12459

    Google Scholar 

  • De Gruyter J, Woudenberg JHC, Aveskamp MM, Verkley GJM, Groenewald JZ, Crous PW (2010) Systematic reappraisal of species in Phoma section Paraphoma, Pyrenochaeta and Pleurophoma. Mycologia 102:1066–1081. doi:10.3852/09-240

    Article  PubMed  Google Scholar 

  • de Lange ES, Balmer D, Mauch-Mani B, Turlings TCJ (2014) Insect and pathogen attack and resistance in maize and its wild ancestors, the teosintes. New Phytol 204:329–341. doi:10.1111/nph.13005

    Article  Google Scholar 

  • Dhingra OD, Maia CB, Lustosa DC, Mesquita JB (2002) Seedborne pathogenic fungi that affect seedling quality of red angico (Anadenanthera macrocarpa) trees in Brazil. J Phytopathol 150:451–455. doi:10.1046/j.1439-0434.2002.00777.x

    Article  Google Scholar 

  • Di Marco S, Calzarano F, Osti F, Mazzullo A (2004) Pathogenicity of fungi associated with a decay of kiwifruit. Australas Plant Pathol 33:337–342. doi:10.1071/AP04024

    Article  Google Scholar 

  • Eppinga MB, Rietkerk M, Dekker SC, De Ruiter PC, Van der Putten WH (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114:168–176. doi:10.1111/j.2006.0030-1299.14625.x

    Article  Google Scholar 

  • Fitzell RD, Peak CM (1984) The epidemiology of anthracnose disease of mango: inoculum sources, spore production and dispersal. Ann Appl Biol 104:53–59. doi:10.1111/j.1744-7348.1984.tb05586.x

    Article  Google Scholar 

  • Flory SL, Kleczewski N, Clay K (2011) Ecological consequences of pathogen accumulation on an invasive grass. Ecosphere 2:1–12. doi:10.1890/ES11-00191.1

    Article  Google Scholar 

  • Gilbert GS, Parker IM (2006) Invasions and the regulation of plant populations by pathogens. In: Cadotte MW, McMahon SM, Fukami T (eds) Conceptual ecology and invasion biology: reciprocal approaches to nature. Springer, Dordrecht, pp 289–306

    Chapter  Google Scholar 

  • Gilbert GS, Webb CO (2007) Phylogenetic signal in plant pathogen–host range. Proc Natl Acad Sci 104:4979–4983

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gramaje D, Mostert L, Armengol J (2011) Characterization of Cadophora luteo-olivacea and C. melinii isolates obtained from grapevines and environmental samples from grapevine nurseries in Spain. Phytopathol Mediterr 50:112–126. http://dx.doi.org/10.14601/Phytopathol_Mediterr-8723

  • Harrington TC, McNew DL (2003) Phylogenetic analysis places the Phialophora-like anamorph genus Cadophora in the Helotiales. Mycotaxon 87:141–152

    Google Scholar 

  • Hawkes CV (2007) Are invaders moving targets? The generality and persistence of advantages in size, reproduction, and enemy release in invasive plant species with time since introduction. Am Nat 170:832–843. doi:10.1086/522842

    Article  PubMed  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung G-H, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüßler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–822. doi:10.1038/nature05110

    Article  PubMed  CAS  Google Scholar 

  • Jarosz AM, Davelos AL (1995) Effects of disease in wild plant populations and the evolution of pathogen aggressiveness. New Phytol 129:371–387. doi:10.1111/j.1469-8137.1995.tb04308.x

    Article  Google Scholar 

  • Kricsfalusy V, Miller GC (2010) Community ecology and invasion of natural vegetation by Cynanchum rossicum (Asclepiadaceae) in the Toronto region, Canada. Thaiszia J Bot 20:53–70

    Google Scholar 

  • Lamprecht SC, Crous PW, Groenewald JZ, Tewoldemedhin YT, Marasas WFO (2011) Diaporthaceae associated with root and crown rot of maize. IMA Fungus 2:13–24. doi:10.5598/imafungus.2011.02.01.03

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H, Zhang X, Zheng R, Li X, Elmer WH, Wolfe LM, Li B (2014) Indirect effects of non-native Spartina alterniflora and its fungal pathogen (Fusarium palustre) on native saltmarsh plants in China. J Ecol 102:1112–1119. doi:10.1111/1365-2745.12285

    Article  Google Scholar 

  • Malmstrom CM, McCullough AJ, Johnson HA, Newton LA, Borer ET (2005) Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia 145:153–164. doi:10.1007/s00442-005-0099-z

    Article  PubMed  Google Scholar 

  • Mangla S, Inderjit, Callaway RM (2008) Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J Ecol 96:58–67. doi:10.1111/j.1365-2745.2007.01312.x

    Google Scholar 

  • Mihail JD, Taylor SJ (1995) Interpreting variability among isolates of Macrophomina phaseolina in pathogenicity, pycnidium production, and chlorate utilization. Can J Bot 73:1596–1603. doi:10.1139/b95-172

    Article  Google Scholar 

  • Mills KE, Bever JD (1998) Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79:1595. doi:10.2307/176779

    Article  Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627. doi:10.1038/nature01317

    Article  PubMed  CAS  Google Scholar 

  • Mitchell CE, Blumenthal D, Jarošík V, Puckett EE, Pyšek P (2010) Controls on pathogen species richness in plants’ introduced and native ranges: roles of residence time, range size and host traits. Ecol Lett 13:1525–1535. doi:10.1111/j.1461-0248.2010.01543.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Morris WF, Hufbauer RA, Agrawal AA, Bever JD, Borowicz VA, Gilbert GS, Maron JL, Mitchell CE, Parker IM, Power AG, Torchin ME, Vázque DP (2007) Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029. doi:10.1890/06-0442

    Article  PubMed  Google Scholar 

  • Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants. Ecology 88:1210–1224

    Article  PubMed  Google Scholar 

  • Pendergast TH, Burke DJ, Carson WP (2013) Belowground biotic complexity drives aboveground dynamics: a test of the soil community feedback model. New Phytol 197:1300–1310. doi:10.1111/nph.12105

    Article  PubMed  Google Scholar 

  • Power AG, Mitchell CE (2004) Pathogen spillover in disease epidemics. Am Nat 164:S79–S89. doi:10.1086/424610

    Article  PubMed  Google Scholar 

  • Pringle JS (1973) The spread of Vincetoxicum species (Asclepiadaceae) in Ontario. Can Field Nat 87:27–33

    Google Scholar 

  • R Core Development Team (2014) R: A language and environment for statistical computing v. 3.1.0. R Foundation for Statistical Computing, Vienna

  • Rasmann S, Erwin AC, Halitschke R, Agrawal AA (2011) Direct and indirect root defences of milkweed (Asclepias syriaca): trophic cascades, trade-offs and novel methods for studying subterranean herbivory. J Ecol 99:16–25. doi:10.1111/j.1365-2745.2010.01713.x

    Article  CAS  Google Scholar 

  • Rillig MC, Wendt S, Antonovics J, Hempel S, Kohler J, Wehner J, Caruso T (2014) Interactive effects of root endophytes and arbuscular mycorrhizal fungi on an experimental plant community. Oecologia 174:263–270. doi:10.1007/s00442-013-2759-8

    Article  PubMed  Google Scholar 

  • Sanderson LA, Antunes PM (2013) The exotic invasive plant Vincetoxicum rossicum is a strong competitor even outside its current realized climatic temperature range. NeoBiota 16:1–15. doi:10.3897/neobiota.16.4012

    Article  Google Scholar 

  • Schäfer W, Straney D, Ciuffetti L, Van Etten HD, Yoder OC (1989) One enzyme makes a fungal pathogen, but not a saprophyte, virulent on a new host plant. Science 246:247–249. doi:10.1126/science.246.4927.247

    Article  PubMed  Google Scholar 

  • Scott PM (1913) The seed plants of Toronto and vicinity. In: Faull JH (ed) The natural history of the Toronto Region. The Canadian Institute, Toronto, pp 100–140

    Google Scholar 

  • Smiley RW, Fowler MC (1984) Leptosphaeria korrae and Phialophora graminicola associated with Fusarium blight syndrome of Poa pratensis in New York. Plant Dis 68:440–442. doi:10.1094/PD-68-440

    Article  Google Scholar 

  • Sun H, Zhang J-Z (2009) Colletotrichum destructivum from cowpea infecting Arabidopsis thaliana and its identity to C. higginsianum. Eur J Plant Pathol 125:459–469. doi:10.1007/s10658-009-9495-2

    Article  Google Scholar 

  • Tomioka K, Sato T, Moriwaki J, Terasawa Y, Koganezawa H (2012) Anthracnose of bacopa caused by Colletotrichum destructivum. J Gen Plant Pathol 78:133–135. doi:10.1007/s10327-011-0357-3

    Article  Google Scholar 

  • Waite TA, Campbell LG (2006) Controlling the false discovery rate and increasing statistical power in ecological studies. Ecoscience 13:439–442. doi:10.2980/1195-6860(2006)13[439:CTFDRA]2.0.CO;2

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribsomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–324

    Google Scholar 

  • Wilson H, Blaisdell GK, Carroll GC, Roy BA (2014) Tall fescue is a potential spillover reservoir host for Alternaria species. Mycologia. doi:10.3852/12-330

    Google Scholar 

  • You Y-H, Yoon H, Kang S-M, Woo J-R, Choo Y-S, Lee I-J, Shin J-H, Kim J-G (2013) Cadophora malorum Cs-8-1 as a new fungal strain producing gibberellins isolated from Calystegia soldanella. J Basic Microbiol 53:630–634. doi:10.1002/jobm.201200002

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q, Yang R, Tang J, Yang H, Hu S, Chen X (2010) Positive feedback between mycorrhizal fungi and plants influences plant invasion success and resistance to invasion. PLoS One 5:e12380–e12380. doi:10.1371/journal.pone.0012380

    Article  PubMed  PubMed Central  Google Scholar 

  • Zolna M, Kierpiec-Baran B, Kowalik M (2013) The diversity of fungi colonizing necrotic inflorescence buds of rhododendron (Rhododendron L.). Acta Agrobot 66:79–84. doi:10.5586/aa.2013.025

    Article  Google Scholar 

Download references

Acknowledgments

We would like to sincerely thank G. J. Boland for helping with fungal identification work and for the use of his facilities. Thank you to R. Dickinson for help with site information and field collections. Thank you to P. Carson for supplying S. canadensis seeds,  M. Mucci, T. Slimmon, B. Collis, J. Drummelsmith, and F. Small for helping with the growth chamber experiments, and to J. Gross and staff at the Genomics Facility at the University of Guelph for performing the Sanger sequencing. Funding was provided by the Natural Sciences and Engineering Research Council of Canada, Ontario Ministry of Natural Resources and Forestry, the New Zealand Federation of Graduate Women Fellowship, the University of Guelph International Graduate Scholarship, and the Ontario Federation of Anglers and Hunters.

Author contributions

NJD, KED and PMA designed the experiments. NJD performed the experiments, statistical analyses, and wrote the first draft. NJD, KED and PMA wrote and edited the manuscript.

Author information

Author notes

  1. Nicola J. Day

    Present address: Biology Department, Wilfrid Laurier University, 75 University Avenue West, Waterloo, ON, N2L 3C5, Canada

Authors and Affiliations

  1. School of Environmental Sciences, University of Guelph, 50 Stone Road East, Guelph, ON, N1G 2W1, Canada

    Nicola J. Day & Kari E. Dunfield

  2. Department of Biology, Algoma University, 1520 Queen Street East, Sault Ste. Marie, ON, P6A 2G4, Canada

    Pedro M. Antunes

Authors
  1. Nicola J. Day
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kari E. Dunfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pedro M. Antunes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pedro M. Antunes.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 110 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Day, N.J., Dunfield, K.E. & Antunes, P.M. Fungi from a non-native invasive plant increase its growth but have different growth effects on native plants. Biol Invasions 18, 231–243 (2016). https://doi.org/10.1007/s10530-015-1004-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-1004-2

Keywords

Search

Navigation