Skip to main content
SpringerLink
Log in

Allelopathic potential of invasive species is determined by plant and soil community context

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

The search for mechanisms to explain the competitive dominance of invasive species has generated much interest in testing for allelopathy as a major mechanism of plant invasion. The Novel Weapons Hypothesis postulates that invasive plants disproportionally impact native plants by producing novel allelochemicals. We studied the allelopathic potential of three invasive and three native species on twelve co-occurring plant species in the Eastern Deciduous Forest of Indiana, USA, using foliar leachate and soil with an intact microbial community. Our bioassay was a full factorial test of two soil treatments and six foliar leachates on the germination and growth of 12 species (2 × 6 × 12 full factorial). The strength of allelopathic impacts were context dependent, with significant 3-way and 2-way interactions between leachate species, target species, and soil microbial communities (live vs. sterilized). Allelopathic potential was different between life stages of the target species. Ligustrum vulgare’s and Lonicera maackii’s impacts on some native species supported the Novel Weapons Hypothesis; however, the invasives as a group did not significantly affect growth and had a weaker effect on germination than the effect of certain invasive species individually. For example, native Cercis canadensis reduced germination and growth in some conditions. Our results in the live soil treatment indicate that some natives, such as Elymus hystrix, should be resistant to Lonicera maackii and Ligustrum vulgare, but these shrubs’ allelopathy could contribute to the decline of susceptible native species.

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

  • Anderson RC, Loucks OL (1966) Osmotic pressure influence in germination tests for antibiosis. Science 152:771–773

    Article  CAS  PubMed  Google Scholar 

  • Bauer JT, Shannon SM, Stoops RE, Reynolds HL (2012) Context dependency of the allelopathic effects of Lonicera maackii on seed germination. Plant Ecol 213:1907–1916

    Article  Google Scholar 

  • Bever JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75:1965–1977

    Article  Google Scholar 

  • Bever JD (2002) Host-specificity of AM fungal population growth rates can generate feedback on plant growth. Plant Soil 244:281–290

    Article  CAS  Google Scholar 

  • Blair AC, Hanson BD, Brunk GR, Marrs RA, Westra P, Nissen SJ, Hufbauer RA (2005) New techniques and findings in the study of a candidate allelochemical implicated in invasion success. Ecol Lett 8:1039–1047

    Article  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  • Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson K, Klironomos JN (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055

    Article  PubMed  Google Scholar 

  • Cipollini D, Dorning M (2008) Direct and indirect effects of conditioned soils and tissue extracts of the invasive shrub, Lonicera maackii, on target plant performance. Castanea 73:166–176

    Article  Google Scholar 

  • Cipollini D, Stevenson R, Cipollini K (2008a) Contrasting direct and indirect effects of allelochemicals from two invasive plants on the performance of a non-mycorrhizal plant. Int J Plant Sci 169:371–375

    Article  Google Scholar 

  • Cipollini D, Stevenson R, Enright S, Eyles A, Bonello P (2008b) Phenolic metabolites in leaves of the invasive shrub, Lonicera maackii, and their potential phytotoxic and anti-herbivore effects. J Chem Ecol 34:144–152

    Article  CAS  PubMed  Google Scholar 

  • Cipollini D, Rigsby CM, Barto EK (2012) Microbes as targets and mediators of allelopathy in plants. J Chem Ecol 38:714–727

    Article  CAS  PubMed  Google Scholar 

  • Dorning M, Cipollini D (2006) Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecol 184:287–296

    Article  Google Scholar 

  • Goodall J, Witkowski ETF, Ammann S, Reinhardt C (2010) Does allelopathy explain the invasiveness of Campuloclinium macrocephalum (pompom weed) in the South African grassland biome? Biol Invasions 12:3497–3512

    Article  Google Scholar 

  • Gould AMA, Gorchov DL (2000) Effects of the exotic invasive shrub Lonicera maackii on the survival and fecundity of three species of native annuals. Am Midland Nat 144:36–50

    Article  Google Scholar 

  • Harnden J, MacDougall AS, Sikes BA (2011) Field-based effects of allelopathy in invaded tallgrass prairie. Botany 89:227–234

    Article  Google Scholar 

  • Haugland E, Brandsaeter LO (1996) Experiments on bioassay sensitivity in the study of allelopathy. J Chem Ecol 22:1845–1859

    Article  CAS  PubMed  Google Scholar 

  • Hutchinson TF, Vankat JL (1997) Invasibility and effects of Amur honeysuckle on southwestern Ohio forests. Conserv Biol 11:1117–1124

    Article  Google Scholar 

  • Inderjit DSO (2003) Ecophysiological aspects of allelopathy. Planta 217:529–539

    Article  CAS  PubMed  Google Scholar 

  • Inderjit BD, Rajeswari MS (2010) Interaction of 8-Hydroxyquinoline with soil environment mediates its ecological function. PLoS ONE 5:e12852

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Inderjit STR, Callaway RM, Pollock JL, Kaur J (2008) Allelopathy and plant invasions: traditional, congeneric, and bio-geographical approaches. Biol Invasions 10:875–890

    Article  Google Scholar 

  • Jäderlund A, Zackrisson O, Nilsson MC (1996) Effects of bilberry (Vaccinium myrtillus L.) litter on seed germination and early seedling growth of four boreal tree species. J Chem Ecol 22(5):973–986

    Article  PubMed  Google Scholar 

  • Jäderlund A, Zackrisson O, Dahlberg A, Nilsson MC (1997) Interference of Vaccinium myrtillus on establishment, growth, and nutrition of Picea abies seedlings in northern boreal site. Can J Forest Res 27(12):2017–2025

    Article  Google Scholar 

  • Kaur H, Kaur R, Kaur S, Baldwin IT, Inderjit (2009) Taking ecological function seriously: soil microbial communities can obviate allelopathic effects of released metabolites. PLoS ONE 4(3):e4700

    Article  PubMed Central  PubMed  Google Scholar 

  • Koide RT, Li M (1989) Appropriate controls for vesicular–arbuscular mycorrhiza research. New Phytol 111:35–44

    Article  Google Scholar 

  • Krogmeier MJ, Bremner JM (1989) Effects of phenolic acids on seed germination and seedling growth in soil. Biol Fertil Soils 8:116–122

    Article  CAS  Google Scholar 

  • Larimer AL, Bever JD, Clay K (2012) Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos 121:2090–2096

    Article  Google Scholar 

  • McEwan RW, Rieske LK, Arthur MA (2009) Potential interactions between woody shrubs and the gypsy moth (Lymantria dispar), an invasive insect herbivore. Biol Invasions 11:1053–1058

    Article  Google Scholar 

  • McEwan RW, Arthyr-Paratley LG, Rieske LK, Arthur MA (2010) A multi-assay comparison of seed germination inhibition by Lonicera maackii and co-occurring native shrubs. Flora 205:475–483

    Article  Google Scholar 

  • Merriam RW, Feil E (2002) The potential impact of an introduced shrub on native plant diversity and forest regeneration. Biol Invasions 4:369–373

    Article  Google Scholar 

  • Miller J (2003) Nonnative invasive plants of sourthern forests: a field guide for identification and control. Gen. Tech. Rep. SRS-62. USDA, Forest Service, Southern Research Station, Asheville, NC

    Google Scholar 

  • Morris LL, Walck JL, Hidayati SN (2002) Growth and reproduction of the invasive Ligustrum sinense and native Forestiera ligustrina (Oleaceae): implications for the invasion and persistence of a nonnative shrub. Int J Plant Sci 163:1001–1010

    Article  Google Scholar 

  • Nilsson M-C, Zackrisson O (1992) Inhibition of Scots pine seedling establishment by Empetrum hermaphroditum. J Chem Ecol 18:1857–1870

    Article  CAS  PubMed  Google Scholar 

  • Orr SP, Rudgers JA, Clay K (2005) Invasive plants can inhibit native tree seedlings: testing potential allelopathic mechanisms. Plant Ecol 181:153–165

    Article  Google Scholar 

  • Pisula NL, Meiners SJ (2010) Relative allelopathic potential of invasive plant species in a young disturbed woodland. J Torrey Bot Soc 137:81–87

    Article  Google Scholar 

  • Pollock JL, Callaway RM, Thelen GC, Holben WE (2009) Catechin-metal interactions as a mechanism for conditional allelopathy by the invasive plant, Centaurea maculosa. J Ecol 97:1234–1242

    Article  CAS  Google Scholar 

  • Rice EL (1984) Allelopathy. Academic Press, Orlando, FL

    Google Scholar 

  • R Core Team (2012). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/

  • Shannon S, Flory SL, Reynolds H (2012) Competitive context alters plant-soil feedback in an experimental woodland community. Oecologia 169:235–243

    Article  PubMed  Google Scholar 

  • Stowe LG (1979) Allelopathy and its influence on the distribution of plants in an Illinois old-field. J Ecol 67:1065–1085

    Article  CAS  Google Scholar 

  • Svensson JR, Nylund GM, Cervin G, Toth GB, Pavia H (2013) Novel chemical weapon of an exotic macroalga inhibits recruitment of native competitors in the invaded range. J Ecol 101:140–148

    Article  CAS  Google Scholar 

  • Tharayil N, Bhowmik PC, Xing B (2006) Preferential sorption of phenolic phytotoxins to soil: implications for altering the availability of allelochemicals. J Agric Food Chem 54:3033–3040

    Article  CAS  PubMed  Google Scholar 

  • Wardle DA, Nilsson MC, Gallet C, Zackrisson O (1998) An ecosystem level perspective of allelopathy. Biol Rev 73:305–319

    Article  Google Scholar 

  • Williamson GB (1990) Allelopathy, Koch’s postulates, and the neck riddle. In: Grace JB, Tilman D (eds) Perspectives on plant competition. Academic Press, San Diego, pp 143–162

    Chapter  Google Scholar 

  • Zhu X, Zhang J, Ma K (2011) Soil biota reduce allelopathic effects of the invasive Eupatorium adenophorum. PLoS ONE 6:e25393

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the large number of people who made this work possible, including Heather Reynolds, Rebecca Stoops, Maia Eubanks, Kit Hang-Chan, and all the other members of the Reynolds Lab. Nine reviewers contributed to the final paper with Reviewers 1, 2, and 7 providing particularly helpful suggestions. Stephanie Dickinson and Thomas Jackson at the Indiana Statistical Consulting Center provided invaluable statistical advice.

Author information

Authors and Affiliations

  1. Indiana University, 1001 East Third Street, Bloomington, IN, 47405, USA

    Sarah Shannon-Firestone & Jeffrey Firestone

  2. University of Maryland, 2229 Biology-Psychology Bldg., College Park, MD, 20742, USA

    Jeffrey Firestone

Authors
  1. Sarah Shannon-Firestone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeffrey Firestone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sarah Shannon-Firestone.

Additional information

Communicated by Lara Souza.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 105 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shannon-Firestone, S., Firestone, J. Allelopathic potential of invasive species is determined by plant and soil community context. Plant Ecol 216, 491–502 (2015). https://doi.org/10.1007/s11258-015-0453-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-015-0453-0

Keywords

Search

Navigation