Arthropod-Plant Interactions

, Volume 10, Issue 5, pp 383–391 | Cite as

Costs of induced defenses for the invasive plant houndstongue (Cynoglossum officinale L.) and the potential importance for weed biocontrol

  • Justin B. Runyon
  • Jennifer L. Birdsall
Original Paper


Inducible plant defenses—those produced in response to herbivore feeding—are thought to have evolved as a cost-saving tactic that allows plants to enact defenses only when needed. The costs of defense can be significant, and loss of plant fitness due to commitment of resources to induced defenses could affect plant populations and play a role in determining the success or failure of weed biocontrol. We used methyl jasmonate (MeJA) to experimentally induce defenses without herbivores in invasive houndstongue plants (Cynoglossum officinale L.) in the field and measured resulting growth and fitness (plant size, seed number, and seed weight). MeJA-treated plants emitted large amounts of plant volatiles and produced leaves with twice as many trichomes as untreated plants. Plants with activated defenses had fewer leaves, were smaller, and produced nutlets that weighed less than plants not investing in defenses. These data indicate that herbivore-induced defenses are costly for houndstongue plants in their invaded range and represent significant indirect costs of herbivory beyond direct feeding damage (e.g., loss of photosynthetic tissue). Notably, the magnitude of defenses elicited upon feeding varies greatly by herbivore species and a better understanding of the costs of defense could help us predict which potential biocontrol herbivores are most likely to be effective.


Induced plant defenses Costs Biological control Efficacy Invasive plant Herbivore Cynoglossum officinale 



We thank Thomas O’Neil and Casey M. Delphia for assistance in the field and lab. Casey Delphia, Deb Finch, and three anonymous reviewers provided helpful comments on the manuscript. Reggie Clark and John Councilman (Gallatin National Forest) generously helped find and allowed access to the field sites. This project was supported by funding from PECASE (President’s Early Career Award in Science and Engineering) to Justin Runyon and the Rocky Mountain Research Station, USDA Forest Service.


  1. Accamando AK, Cronin JT (2012) Costs and benefits of jasmonic acid induced responses in soybean. Environ Entomol 41:551–561CrossRefPubMedGoogle Scholar
  2. Agren J, Schemske DW (1993) The cost of defense against herbivores: an experimental study of trichome production in Brassica rapa. Am Nat 141:338–350CrossRefPubMedGoogle Scholar
  3. Aharoni A, Giri AP, Deuerlein S et al (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866–2884CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baker DC, Smart RA, Ralphs M et al (1989) Hounds-tongue (Cynoglossum officinale) poisoning in a calf. J Am Vet Med A 194:929–930Google Scholar
  5. Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci USA 95:8113–8118CrossRefPubMedPubMedCentralGoogle Scholar
  6. Baldwin IT (2001) An ecologically motivated analysis of plant-herbivore interactions in native tobacco. Plant Physiol 127:1449–1458CrossRefPubMedPubMedCentralGoogle Scholar
  7. Baldwin IT, Schmelz EA, Zhang ZP (1996) Effects of octadecanoid metabolites and inhibitors on induced nicotine accumulation in Nicotiana sylvestris. J Chem Ecol 22:61–74CrossRefPubMedGoogle Scholar
  8. Berger U, Piou C, Schiffers K et al (2008) Competition among plants: concepts, individual-based modelling approaches, and a proposal for a future research strategy. Perspect Plant Ecol 9:121–135CrossRefGoogle Scholar
  9. Burkle LA, Runyon JB (2016) Drought and leaf herbivory influence floral volatiles and pollinator attraction. Glob Change Biol 22:1644–1654CrossRefGoogle Scholar
  10. Carson WP, Hovick SM, Baumert AJ, Bunker DE, Pendergast TH (2008) Evaluating the post-release efficacy of invasive plant biocontrol by insects: a comprehensive approach. Arthropod Plant Interact 2:77–86CrossRefGoogle Scholar
  11. Carvalheiro LG, Buckley YM, Ventim R et al (2008) Apparent competition can compromise the safety of highly specific biocontrol agents. Ecol Lett 11:690–700CrossRefPubMedGoogle Scholar
  12. Cipollini DF (2002) Does competition magnify the fitness costs of induced responses in Arabidopsis thaliana? A manipulative approach. Oecologia 131:514–552CrossRefGoogle Scholar
  13. Cipollini D (2007) Consequences of the overproduction of methyl jasmonate on seed production, tolerance to defoliation and competitive effect and response of Arabidopsis thaliana. New Phytol 173:146–153CrossRefPubMedGoogle Scholar
  14. Cipollini D, Lieurance DM (2012) Expression and costs of induced defense traits in Alliaria petiolata, a widespread invasive plant. Basic Appl Ecol 13:432–440CrossRefGoogle Scholar
  15. Crawley MJ (1989) The successes and failures of weed biocontrol using insects. Biocontrol News Inf 10:213–223Google Scholar
  16. Dodd AP (1940) The biological campaign against prickly pear. Commonwealth Prickly Pear Board Bulletin, BrisbaneGoogle Scholar
  17. Eigenbrode SD, Andreas JE, Cripps MG et al (2008) Induced chemical defenses in invasive plants: a case study with Cynoglossum officinale L. Biol Invasions 10:1373–1379CrossRefGoogle Scholar
  18. Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gershenzon J (1994) Metabolic costs of terpenoid accumulation in higher-plants. J Chem Ecol 20:1281–1328CrossRefPubMedGoogle Scholar
  20. Halitschke R, Kessler A, Kahl J et al (2000) Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata. Oecologia 124:408–417CrossRefGoogle Scholar
  21. Halitschke R, Stenberg JA, Kessler D et al (2008) Shared signals—‘alarm calls’ from plants increase apparency to herbivores and their enemies in the field. Ecol Lett 11:24–34PubMedGoogle Scholar
  22. Hare JD, Elle E, van Dam NM (2003) Costs of glandular trichomes in Datura wrightii: a three-year study. Evolution 57:793–805CrossRefPubMedGoogle Scholar
  23. Harris P, Shorthouse JD (1996) Effectiveness of gall inducers in weed biological control. Can Entomol 128:1021–1055CrossRefGoogle Scholar
  24. Heil M (2002) Ecological costs of induced resistance. Curr Opin Plant Biol 5:345–350CrossRefPubMedGoogle Scholar
  25. Hoballah ME, Kollner TG, Degenhardt J et al (2004) Costs of induced volatile production in maize. Oikos 105:168–180CrossRefGoogle Scholar
  26. Holloway JK, Huffaker CB (1951) The role of Chrysolina gemellata in biological control of Klamath weed. J Econ Entomol 44:244–247CrossRefGoogle Scholar
  27. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66CrossRefPubMedGoogle Scholar
  28. Huffaker CB, Holloway JK (1949) Changes in range plant population structure associated with feeding of imported enemies of Klamath weed (Hypericum perforatum L.). Ecology 30:167–175CrossRefGoogle Scholar
  29. Julien MH (1989) Biological control of weeds worldwide: trends, rates of success and the future. Biocontrol News Inf 10:299–306Google Scholar
  30. Kaplan I, Dively GP, Denno RF (2009) The costs of anti-herbivore defense traits in agricultural crop plants: a case study involving leafhoppers and trichomes. Ecol Appl 19:864–872CrossRefPubMedGoogle Scholar
  31. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  32. Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant–pollinator interactions. Ecology 92:1769–1780CrossRefPubMedGoogle Scholar
  33. Knight AP, Kimberling CV, Stermitz FR et al (1984) Cynoglossum officinale (hounds-tongue)—a cause of pyrrolizidine alkaloid poisoning in horses. J Am Vet Med A 185:647–650Google Scholar
  34. Mauricio R (1998) Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am Nat 151:20–28CrossRefPubMedGoogle Scholar
  35. McFadyen REC (1998) Biological control of weeds. Annu Rev Entomol 43:369–393CrossRefPubMedGoogle Scholar
  36. Moles AT, Westoby M (2004) Seedling survival and seed size: a synthesis of the literature. J Ecol 92:372–383CrossRefGoogle Scholar
  37. Morin L, Reid AM, Sims-Chilton NM et al (2009) Review of approaches to evaluate the effectiveness of weed biological control agents. Biol Control 51:1–15CrossRefGoogle Scholar
  38. Moyer JR, DeClerck-Floate RA, Van Hezewik BH et al (2007) Agronomic practices for growing houndstongue (Cynogiossum officinale) as a crop for mass-producing a weed biocontrol agent. Weed Sci 55:273–280CrossRefGoogle Scholar
  39. Nabity PD, Zavala JA, DeLucia EH (2009) Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Ann Bot 103:655–663CrossRefPubMedGoogle Scholar
  40. Pearson DE, Callaway RM (2005) Indirect nontarget effects of host-specific biological control agents: implications for biological control. Biol Control 35:288–298CrossRefGoogle Scholar
  41. Redman AM, Cipollini DF, Schultz JC (2001) Fitness costs of jasmonic acid-induced defense in tomato, Lycopersicon esculentum. Oecologia 126:380–385CrossRefGoogle Scholar
  42. Robert CAM, Erb M, Hiltpold I et al (2013) Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field. Plant Biotechnol J 11:628–639CrossRefPubMedGoogle Scholar
  43. Runyon JB, Mescher MC, De Moraes CM (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–1967CrossRefPubMedGoogle Scholar
  44. Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiol 146:845–851CrossRefPubMedPubMedCentralGoogle Scholar
  45. Schwinning S, Weiner J (1998) Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia 113:447–455CrossRefGoogle Scholar
  46. Sletvold N, Huttunen P, Handley R et al (2010) Cost of trichome production and resistance to a specialist insect herbivore in Arabidopsis lyrata. Evol Ecol 24:1307–1319CrossRefGoogle Scholar
  47. Steppuhn A, Baldwin IT (2008) Induced defenses and the cost-benefit paradigm. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Berlin, pp 61–83CrossRefGoogle Scholar
  48. Thaler JS, Stout MJ, Karban R et al (2001) Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol Entomol 26:312–324CrossRefGoogle Scholar
  49. Tooker JF, De Moraes CM (2009) A gall-inducing caterpillar species increases essential fatty acid content of its host plant without concomitant increases in phytohormone levels. Mol Plant Microbe Interact 22:551–559CrossRefPubMedGoogle Scholar
  50. Tooker JF, De Moraes CM (2011) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling. J Plant Growth Regul 30:158–165CrossRefGoogle Scholar
  51. Tooker JF, Helms AM (2014) Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habit. J Chem Ecol 40:742–753CrossRefPubMedGoogle Scholar
  52. Tooker JF, Rohr JR, Abrahamson WG et al (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671CrossRefPubMedGoogle Scholar
  53. Upadhyaya MK, Tilsner HR, Pitt MD (1988) The biology of Canadian weeds. 87. Cynoglossum officinale L. Can J Plant Sci 68:763–774CrossRefGoogle Scholar
  54. Van Dam NM, Baldwin IT (2001) Competition mediates costs of jasmonate-induced defences, nitrogen acquisition and transgenerational plasticity in Nicotiana attenuata. Funct Ecol 15:406–415CrossRefGoogle Scholar
  55. van Klinken RD, Raghu S (2006) A scientific approach to agent selection. Aust J Entomol 45:253–258CrossRefGoogle Scholar
  56. Zangerl AR, Hamilton JG, Miller TJ et al (2002) Impact of folivory on photosynthesis is greater than the sum of its holes. Proc Natl Acad Sci USA 99:1088–1091CrossRefPubMedPubMedCentralGoogle Scholar
  57. Zavala JA, Patankar AG, Gase K et al (2004) Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. Proc Natl Acad Sci USA 101:1607–1612CrossRefPubMedPubMedCentralGoogle Scholar
  58. Zuest T, Joseph B, Shimizu KK et al (2011) Using knockout mutants to reveal the growth costs of defensive traits. Proc R Soc B Biol Sci 278:2598–2603CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2016

Authors and Affiliations

  1. 1.Rocky Mountain Research Station, Forestry Sciences LaboratoryUSDA Forest ServiceBozemanUSA

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