Skip to main content

Herbivory and novel weapons: no evidence for enhanced competitive ability or allelopathy induction of Centaurea diffusa by biological controls

Biological Invasions volume 10, Article number: 79 (2008) Cite this article

Abstract

Biological control of weeds by arthropod herbivores is thought to work by reducing the competitive ability of the weed relative to the surrounding vegetation. However, the assumption that herbivory reduces plant competitive ability has not been tested in most biological control systems, and counter to expectation, recent research on the impact of biological control agents on invasive Centaurea species suggests that this genus may respond to herbivory by increased competitive ability through enhanced plant re-growth and/or by inducing increased production of phytotoxic allelochemicals. We examined the impact of two biological control agents of the invasive plant diffuse knapweed (C. diffusa) to see if feeding by either of these insects would enhance the plant’s competitive ability or allelochemical output. Sub-lethal herbivory by either of the biological control agents significantly reduced knapweed performance when the plant was grown in competition with either of two native species. Competition with knapweed significantly reduced the performance of both native species (Artemisia frigida and Bouteloua gracilis), and herbivory by one of the biocontrol agents resulted in a small but significant increase in both native species’ performance. Diffuse knapweed’s putative allelochemical 8-hydroxyquinoline was not detected in experimental or field collected soils from knapweed-infested sites. In contrast to other studies on the impacts of biological control on other Centaurea species, these data support the premise that biological control agents may reduce invading plant competitive ability. We find no evidence for diffuse knapweed allelopathy mediated by 8-hydroxyquinoline or enhanced allelopathy in response to herbivory by biological control agents.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3

References

  • Andres LA, Goeden RD (1971) Biological control of weeds by introduced natural enemies. In: Huffaker C (ed) Biological control: proceedings of an AAAS symposium on biological control. Plenum, New York

    Google Scholar 

  • Baiocchi C, Saini G, Bertolo P, Cartoni GP, Pettiti G (1988) Pre-column chelation with 8-hydroxyquinoline for the simultaneous determination of metal-ions by reversed-phase high performance liquid-chromatography. Analyst 113(5):805–807

    Article  CAS  Google Scholar 

  • Bais HP, Walker TS, Stermitz FR, Hufbauer RA, Vivanco J (2002) Entantiomeric-dependant phytotoxic and antimicrobial activity of (±)-catechin, a rhizosecreted racemic mixture from spotted knapweed. Plant Physiol 128(4):1173–1179

    PubMed  Article  CAS  Google Scholar 

  • Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380

    PubMed  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(10):1039–1047

    Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2(8):436–443

    Article  Google Scholar 

  • Callaway RM, DeLuca TH, Belliveau WM (1999) Herbivores used for biological control may increase the competitive ability of the noxious weed Centaurea maculosa. Ecology 80(4):1196–1201

    Google Scholar 

  • Callaway RM, Kim J, Mahall BE (2006) Defoliation of Centaurea solstitialis stimulates compensatory growth and intensifies negative effects on neighbors. Biol Invasions 8:1389–1397

    Article  Google Scholar 

  • Coombs EM, Clark JK, Piper GL, Cofrancesco AF Jr (eds) (2004) Biological control of invasive plants in the United States. Oregon State University Press, Corvallis

    Google Scholar 

  • Denoth M, Myers JH (2005) Variable success of biological control of Lythrum salicaria in British Columbia. Biol Control 32(2):269–279

    Article  Google Scholar 

  • Denoth M, Frid L, Myers JH (2002) Multiple agents in biological control: improving the odds? Biol Control 24:20–30

    Article  Google Scholar 

  • Duncan CL (2001) Knapweed management: another decade of change. In: Smith L (ed) Proceedings, 1st international knapweed symposium of the 21st century. March 15–16, Coeur d’Alene, Idaho. U.S. Department of Agriculture, Agricultural Research Service, Albany

  • Hajek AE (2004) Natural enemies: an introduction to biological control. Cambridge University Press, Cambridge

    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(1):5–15

    Article  Google Scholar 

  • Julien MH, Griffiths MW (1998) Biological control of weeds. A world catalogue of agents and their target weeds, 4th edn. CABI Publishing, Wallingford

    Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17(4):164–170

    Article  Google Scholar 

  • LeJeune KD, Suding KN, Sturgis S, Scott A, Seastedt TR (2005) Biological control insect use of fertilized and unfertilized diffuse knapweed in a Colorado grassland. Environ Entomol 34(1):225–234

    Article  Google Scholar 

  • Maschinski J, Whitham TG (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability and timing. Am Nat 134:1–19

    Article  Google Scholar 

  • Müller-Schärer H (1991) The impact of root herbivory as a function of plant density and competition: survival, growth and fecundity of Centaurea maculosa in field plots. J Appl Ecol 28:759–776

    Article  Google Scholar 

  • Newingham BA, Callaway RM (2006) Shoot herbivory on the invasive plant, Centaurea maculosa, does not reduce its competitive effects on conspecifics and natives. Oikos 114:397–406

    Article  Google Scholar 

  • Ridenour WM, Callaway RM (2003) Root herbivores, pathogenic fungi, and competition between Centaurea maculosa and Festuca idahoensis. Plant Ecol 169:161–170

    Article  Google Scholar 

  • Rosenthal JP, Kotanen PM (1994) Terrestrial plant tolerance to herbivory. Trends Ecol Evol 9(4):145–148

    Article  Google Scholar 

  • SAS Institute (2002) JMP, version 5. SAS Institute Inc., Cary

    Google Scholar 

  • Steinger T, Müller-Schärer H (1992) Physiological and growth response of Centaurea maculosa (Asteraceae) to root herbivory under varying levels of interspecific plant competition and soil nitrogen availability. Oecologia 91:141–149

    Google Scholar 

  • Stermitz FR, Bais HP, Foderaro TA, Vivanco JM (2003) 7,8-Benzoflavone: a phytotoxin from root exudates of invasive Russian knapweed. Phytochemistry 64:493–497

    PubMed  Article  CAS  Google Scholar 

  • Thaler JS, Stout MJ, Karban R, Duffey SS (2001) Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol Entomol 26:312–324

    Article  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 Lett 8:209–217

    Article  Google Scholar 

  • USDA, NRCS (2006) The PLANTS Database, 6 March 2006 (http://plants.usda.gov). Data compiled from various sources by Mark W. Skinner. National Plant Data Center, Baton Rouge

  • Vivanco JM, Bais HP, Stermitz FR, 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 

  • Weber WA, Wittmann RC (2001) Colorado flora: eastern slope, 3rd edn. University Press of Colorado, Boulder

    Google Scholar 

  • Zouhar K (2001) Centaurea diffusa. In: Fire effects information system, [Online]. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory (Producer). Available: http://www.fs.fed.us/database/feis/ [2006, March 7]

Download references

Acknowledgments

We would like to thank Heather Batts, Emily Sadler, Todd Green, and Nathan Kirkley for assistance in plant harvests. This research was greatly improved through continual group discussions with Cynthia Brown, Helen Rowe, Erin Bard, Hilary Drucker, Ruth Hufbauer, Steve Rauth, Dan McKinnon, Robin Marrs, and Dan Cariveau. The manuscript was greatly improved by thoughtful comments from three anonymous reviewers. This research was funded by a Colorado State University Agricultural Experiment Station grant to APN. All experiments and analyses conducted comply with current US laws.

Author information

Authors and Affiliations

  1. Department of Bioagricultural Sciences and Pest Management and Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO, 80523-1177, USA

    Andrew P. Norton & Amy C. Blair

  2. Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, 80523-1177, USA

    Janet G. Hardin, Scott J. Nissen & Galen R. Brunk

Authors
  1. Andrew P. Norton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amy C. Blair
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Janet G. Hardin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Scott J. Nissen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Galen R. Brunk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew P. Norton.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Norton, A.P., Blair, A.C., Hardin, J.G. et al. Herbivory and novel weapons: no evidence for enhanced competitive ability or allelopathy induction of Centaurea diffusa by biological controls. Biol Invasions 10, 79 (2008). https://doi.org/10.1007/s10530-007-9111-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10530-007-9111-3

Keywords

  • Novel weapons
  • Interspecific competition
  • 8-Hydroxyquinoline
  • Centaurea diffusa
  • Bouteloua gracilis
  • Artemisia frigida
  • Indirect effects
  • Non-target impacts
  • Allelochemical induction