Skip to main content
SpringerLink
Log in

Biogeographic differences in the effects of Centaurea stoebe on the soil nitrogen cycle: novel weapons and soil microbes

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

Abstract

The success of some invasive plants may be due in part to native organisms lacking adaptation to species-specific biochemical traits of invaders—the Novel Weapons Hypothesis. We tested this hypothesis in the context of soil microbial communities by comparing the effects of Centaurea stoebe and the root exudate (±)-catechin, on ammonification and nitrification in both the non-native and native ranges of this species. In a non-native range (Montana), soil nitrate (NO3 −) concentrations were lower in invaded than uninvaded grasslands. This did not appear to be due only to higher uptake rates as both C. stoebe plants and catechin significantly reduced resin extractable NO3 −, the maximum rate of nitrification, and gross nitrification in Montana soils. Thus, reduced NO3 − in invaded communities may be due in part to the inhibition of nitrifying bacteria by secondary metabolites produced by C. stoebe. The effects of C. stoebe on N-related processes were different in Romanian grasslands, where C. stoebe is native. In Romanian soil, C. stoebe had no effect on resin extractable NH4 + or NO3 − (compared to other plant species), the maximum rate of nitrification, nor gross nitrification. A relatively high concentration of catechin reduced the maximum rate of nitrification in situ, but substantially less than in Montana. In vivo, gross ammonification was lowest when treated with catechin. Our results suggest biogeographic differences in the way a plant species alters nitrogen cycling through the direct effects of root exudates and adds to a growing body of literature demonstrating the important belowground effects 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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arunachalam M, Monhan N, Mahadevan A (2003) Cloning of Acinetobacter calcoaceticus chromosomal region involved in catechin degradation. Microbiol Res 158:37–46

    Article  PubMed  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 Letts 8:1039–1047

    Article  Google Scholar 

  • Blair AC, Nissen SJ, Brunk GR, Hufbauer RA (2006) Lack of evidence for an ecological role of the putative allelochemical (±)-catechin in spotted knapweed invasion success. J Chem Ecol 32:2327–2331

    Article  PubMed  CAS  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523

    Article  PubMed  CAS  Google Scholar 

  • Callaway RM, Hierro JL (2005) Resistance and susceptibility of plant communities to invasion: revisiting Rabotnov’s ideas about community homeostasis. In: Reigosa MJ, Pedrol N, Gonzalez L (eds) Allelopathy: a physiological process with ecological implications. Springer, The Netherlands, pp 395–414

    Google Scholar 

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

    Article  Google Scholar 

  • Callaway RM, Thelen GC, Barth S, Ramsey PW, Gannon JE (2004a) Soil fungi alter interactions between North American plant species and the exotic invader Centaurea maculosa in the field. Ecology 85:1062–1071

    Article  Google Scholar 

  • Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004b) Release from inhibitory soil biota in Europe and positive plant-soil feedbacks in North America promote invasion. Nature 427:731–733

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Chen BM, Peng SL, Ni G (2009) Effects of the invasive plant Mikania micrantha H.B.K. on soil nitrogen availability through allelopathy in South China. Biol Invasions 11:1291–1299

    Article  Google Scholar 

  • Chobot V, Huber C, Trettnhahn G, Hadacek F (2009) (±)-Catechin: Chemical weapon or stress regulator? J Chem Ecol 35:980–996

    Article  PubMed  CAS  Google Scholar 

  • DeLuca TH, Mackenzie D, Gundale MJ (2006) Biochar effects on soil nutrient transformations. In: Lehmann J, Joseph S (eds) Biochar for environmental management: science and technology. Earthscan, London, pp 252–270

    Google Scholar 

  • Duke SO, Blair AC, Dayan FE, Johnson RD, Meepangala KM, Cook D, Bajsa J (2009) Is (−)-catechin a novel weapon of spotted knapweed (Centaurea stoebe)? J Chem Ecol 35:141–153

    Article  PubMed  CAS  Google Scholar 

  • Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523

    Article  CAS  Google Scholar 

  • Ehrenfeld JG, Kourtev P, Huang W (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–1300

    Article  Google Scholar 

  • Hart SC, Nason GE, Myrold DD, Perry DA (1994a) Dynamics of gross nitrogen transformations in an old-growth forest: the carbon connection. Ecology 75:880–891

    Article  Google Scholar 

  • Hart SC, Stark JM, Davidson EA, Firestone MK (1994b) Nitrogen mineralization, immobilization and nitrification. In: Weaver RW, Angle JS, Bottomley PS (eds) Methods of soil analysis. Part 2: microbiological and biochemical properties. Soil Science Society of America, Madison, pp 985–1017

    Google Scholar 

  • Hawkes CV, Wren EF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985

    Article  Google Scholar 

  • He W, Feng Y, Ridenour RM, Thelen GC, Diaconu A, Callaway RM (2009) Novel weapons and invasion: biogeographic differences in competitive effects of Centaurea maculosa and its root exudate (±)-catechin. Oecologia 159:803–815

    Article  PubMed  Google Scholar 

  • Herron GJ (2001) Influence of nutrient availability on the interaction between spotted knapweed and bluebunch wheatgrass. Restor Ecol 9:326–331

    Article  Google Scholar 

  • Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15

    Article  Google Scholar 

  • Hook PB, Olson BE, Wraith JM (2004) Effects of the invasive forb on grassland carbon and nitrogen pools in Montana, USA. Ecosystems 7:686–694

    Article  CAS  Google Scholar 

  • Inderjit PJL, Callaway RM, Holben W (2008) Phytotoxic effects of (±)-catechin in vitro, in soil, and in the field. PLoS ONE 3:e2536. doi:10.1371/journal.pone.0002536

    Article  PubMed  CAS  Google Scholar 

  • Inderjit KR, Kaur S, Callaway RM (2009) Impact of (±)-catechin on soil microbial communities. Commun Integ Biol 2:1–3

    Article  Google Scholar 

  • Jacobs JS, Sheley RL, Carter JR (2000) Picloram, fertilizer, and defoliation interactions on spotted knapweed reinvasion. J Range Manag 53:309–314

    Article  Google Scholar 

  • Keeney DR, Nelson DW (1982) Nitrogen-inorganic forms. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2. Chemical and microbiological processes, 2nd edn. Soil Science Society of America, Madison, pp 643–698

    Google Scholar 

  • Kjonaas OJ (1999) In situ efficiency of ion exchange resins in studies of nitrogen transformation. Soil Sci Soc Am J 63:399–409

    Article  CAS  Google Scholar 

  • Lacey JR, Wallander R, Olson-Rutz K (1992) Recovery, germinability, and viability of leafy spurge (Euphorbia esula) seeds ingested by sheep and goats. Weed Technol 6:599–602

    Google Scholar 

  • Lejeune KD, Seastedt TR (2001) Centaurea species: the forb that won the west. Conserv Biol 15:1568–1574

    Article  Google Scholar 

  • Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714

    Article  PubMed  CAS  Google Scholar 

  • Lodhi MAK, Killingbeck KT (1980) Allelopathic inhibition of nitrification and nitrifying bacteria in a ponderosa pine (Pinus ponderosa Dougl.) community. Am J Bot 67:1423–1429

    Article  CAS  Google Scholar 

  • MacKenzie MD, DeLuca TH, Sala A (2006) Fire exclusion and nitrogen mineralization in low elevation forests of western Montana. Soil Biol Biochem 38:952–961

    Article  CAS  Google Scholar 

  • Maddox DM (1979) The knapweeds: their economics and biological control in the western states, USA. Rangelands 1:139–141

    Google Scholar 

  • Mallik AU, Pellissier F (2000) Effects of Vaccinium myrtillus on spruce regeneration: testing the notion of coevolutionary significance of allelopathy. J Chem Ecol 26:2197–2209

    Article  CAS  Google Scholar 

  • Marler MJ, Zabinski CA, Wojtowicz T, Callaway RM (1999) Mycorrhizae and fine root dynamics of Centaurea maculosa and native bunchgrass species in western Montana. Northwest Sci 73:217–224

    Google Scholar 

  • Maron JL, Marler M (2008a) Effects of native species diversity and resource additions on invader impact. Am Nat 172:18–33

    Article  Google Scholar 

  • Maron JL, Marler M (2008b) Field-based competitive impacts between invaders and natives at varying resource supply. J Ecol 96:1187–1197

    Article  Google Scholar 

  • Meiman PJ, Redente EF, Paschke MW (2006) The role of the native soil community in the invasion ecology of spotted (Centaurea maculosa auct. non Lam.) and diffuse (Centaurea diffusa Lam.) knapweed. Appl Soil Ecol 32:77–88

    Article  Google Scholar 

  • Olson BE, Blicker PS (2003) Traits of the invasive Centaurea maculosa and two native grasses: effect of N pulses. Plant Soil 254:457–467

    Article  CAS  Google Scholar 

  • Perry LG, Thelen GC, Ridenour WM, Callaway RM, Paschke MW, Vivanco JM (2007) Concentrations of the allelochemical (±)-catechin in Centaurea maculosa soils. J Chem Ecol 33:2337–2344

    Article  PubMed  CAS  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 

  • Rabotnov TA (1982) Importance of the evolutionary approach to the study of allelopathy. Ékologia 3:5–8

    Google Scholar 

  • Rice EL (1964) Inhibition of nitrogen-fixing and nitrifying bacteria by seed plants (L). Ecology 45:824–837

    Article  Google Scholar 

  • Rice PM, Toney JC, Bedunah DJ, Carlson CE (1997) Plant community diversity and growth form responses to herbicide applications for control of Centaurea maculosa. J Appl Ecol 34:1397–1412

    Article  Google Scholar 

  • Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126:444–450

    Article  Google Scholar 

  • Rout ME, Callaway RM (2009) An invasive plant paradox. Science 324:734–735

    Article  PubMed  CAS  Google Scholar 

  • Schultz MJ (2008) Soil ecological interactions of spotted knapweed and native plant species. M.S. Thesis, Colorado State University, Fort Collins, Colorado

  • Sheley RL, Jacobs JS, Carpinelli MF (1998) Distribution, biology, and management of diffuse knapweed and spotted knapweed. Weed Technol 12:353–362

    Google Scholar 

  • Simoes K, Du J, Kretzschmar FS, Broeckling CD, Stermitz FS, Vivanco JM, Braga MR (2008) Phytotoxic catechin leached by seeds of the tropical weed Sesbania virgata. J Chem Ecol 34:681–687

    Article  PubMed  CAS  Google Scholar 

  • Stark JM, Hart SC (1996) Diffusion technique for preparing salt solutions, Kjedahl digests, and persulfate digests for nitrogen-15 analysis. Soil Sci Soc Am J 60:1846–1855

    Article  CAS  Google Scholar 

  • Stermitz FR, Hufbauer RA, Vivanco JM (2009) Retraction. Enantiomeric-dependent phytotoxic and antimicrobial activity of (±)-catechin. A rhizosecreted racemic mixture from spotted knapweed. Plant Physiol 151:967

    Article  CAS  Google Scholar 

  • Stevenson FJ, Cole MA (1999) Cycles of the soil: carbon, nitrogen, phosphorus, sulfur, micronutrients, 2nd edn. Wiley, New York, p 427

    Google Scholar 

  • Tharayil N, Triebwasser DJ (2010) Elucidation of a diurnal pattern of catechin exudation by Centaurea stoebe. J Chem Ecol 36:200–204

    Article  PubMed  CAS  Google Scholar 

  • Thelen GC, Vivanco JM, Newingham B, Good W, Bais HP, Landres P, Caesar A, Callaway RM (2005) Insect herbivory stimulates allelopathic exudation by an invasive plant and the suppression of natives. Ecol Letts 8:209–217

    Article  Google Scholar 

  • Thibault JR, Fortin JA, Smirnoff WA (1982) In vitro allelopathic inhibition of nitrification by balsam poplar and balsam fir. Am J Bot 69:676–679

    Article  Google Scholar 

  • Thorpe AS (2006) Biochemical effects of Centurea maculosa on soil nutrient cycles and plant communities. PhD dissertation. The University of Montana-Missoula, Missoula, Montana, p 122

  • Thorpe AS, Archer V, DeLuca TH (2006) The invasive forb, Centaurea maculosa, increases available phosphorus availability in Montana grasslands. J Appl Soil Ecol 32:118–122

    Article  Google Scholar 

  • Thorpe AS, Thelen GC, Diaconu A, Callaway RM (2009) Root exudate is allelopathic in invaded community but not in native community: field evidence for the novel weapons hypothesis. J Ecol 97:641–645

    Article  Google Scholar 

  • Tyser RW, Key CH (1988) Spotted knapweed in natural area fescue grasslands: an ecological assessment. Northwest Sci 62:151–160

    Google Scholar 

  • Vitousek PM (1986) Biological invasions and ecosystem properties: can species make a difference? In: Mooney GA, Drake JA (eds) Ecology of biological invasions of North America and Hawaii. Springer, New York, pp 163–178

    Google Scholar 

  • Vitousek PM, Walker LR, Whiteaker LD, Mueller-Dombois D, Matson PA (1987) Biological invasion by Myrica faya in Hawai’i: plant demography, nitrogen fixation, ecosystem effects. Ecol Monogr 59:247–265

    Article  Google Scholar 

  • Vivanco JM, Bais FHP, Stermitz R, Thelen GC, Callaway RM (2004) Biogeographical variation in community response to root allelochemistry: novel weapons and exotic invasion. Ecol Lett 7:285–292

    Article  Google Scholar 

  • Wardle DA, Nilsson M-C, Galle C, Zachrisson O (1998) An ecosystem-level perspective of allelopathy. Biol Rev 73:305–319

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful for funding from the Montana Department of Agriculture Noxious Weeds Trust Fund, John W. Marr Memorial Ecology Fund, and the P.E.O. Sisterhood to A.S.T., and the Aldo Leopold Wilderness Center, the US Department of Agriculture, Department of Defense Strategic Environmental Research and Development Program, International Programs at the National Science Foundation, The Andrew W. Mellon Foundation, and the Civilian Research and Development Foundation to R.M.C. We thank G. Thelen and A. Diaconu for assistance in the field in Montana and Romania, T. Deluca for assistance with nitrogen analyses, and M. Grecu and V. Cosma for translation in Romania.

Author information

Authors and Affiliations

  1. Institute for Applied Ecology, PO Box 2855, Corvallis, OR, 97339-2855, USA

    Andrea S. Thorpe

  2. Division of Biological Sciences, The University of Montana, Missoula, MT, 59812, USA

    Andrea S. Thorpe & Ragan M. Callaway

Authors
  1. Andrea S. Thorpe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ragan M. Callaway
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea S. Thorpe.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thorpe, A.S., Callaway, R.M. Biogeographic differences in the effects of Centaurea stoebe on the soil nitrogen cycle: novel weapons and soil microbes. Biol Invasions 13, 1435–1445 (2011). https://doi.org/10.1007/s10530-010-9902-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-010-9902-9

Keywords

Search

Navigation