Skip to main content

Advertisement

Log in

Soil nitrogen availability and herbivore attack influence the chemical defenses of an invasive plant (Linaria dalmatica; Plantaginaceae)

  • Research Paper
  • Published:
Chemoecology Aims and scope Submit manuscript

Abstract

Chemical defenses are thought to contribute to the invasion success and impacts of many introduced plants; however, for most of these species, little is known about these compounds and how they vary in natural environments. Plant allelochemical concentrations may be affected by a variety of abiotic and biotic factors, including soil nutrients and herbivores. Moreover, such quantitative variation is likely to play an important role in species interactions involving these invasive plants. The purpose of this study was to examine patterns of variation in iridoid glycoside concentrations of the invasive plant Linaria dalmatica (Plantaginaceae). We conducted a greenhouse experiment to investigate the effect of soil nitrogen availability on iridoid glycoside concentrations. Results from this experiment showed that plant iridoid glycoside concentrations decreased with increased nitrogen availability. Additionally, plants were collected from multiple field sites in order to characterize the influence of population, soil nitrogen availability, and herbivore attack on iridoid glycoside variation. Results from field studies indicated that plants demonstrated considerable seasonal variation, as well as variation within and among populations, with iridoid glycoside concentrations ranging from approximately 1 to 15% dry weight. The relationship between soil nitrogen and plant iridoid glycosides varied among populations, with a strong negative correlation in one population, a marginally significant negative relationship in a second population, and no relationship in the remaining two populations. Additionally, we found a negative relationship between iridoid glycoside concentrations and plant injury by an introduced biocontrol agent, the stem-mining weevil Mecinus janthinus (Cucurlionidae). These results show that plant allelochemical concentrations can vary widely in natural environments and suggest that levels of plant defense may be reduced by increased soil nitrogen availability and herbivore attack in this invasive plant species.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adler LS, Schmitt J, Bowers MD (1995) Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75–85

    Article  Google Scholar 

  • Alex JF (1962) The taxonomy, history, and distribution of Linaria dalmatica. Can J Bot 40:295–307

    Article  Google Scholar 

  • Barton KE (2007) Early ontogenetic patterns in chemical defense in Plantago (Plantaginaceae): Genetic variation and trade-offs. Am J Bot 94:56–66

    Article  PubMed  CAS  Google Scholar 

  • Barton KE (2008) Phenotypic plasticity in seedling defense strategies: compensatory growth and chemical induction. Oikos 117:917–925

    Article  Google Scholar 

  • Barton KE, Bowers MD (2006) Neighbor species differentially alter resistance phenotypes in Plantago. Oecologia 150:442–452

    Article  PubMed  Google Scholar 

  • Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67

    Article  Google Scholar 

  • Beninger CW, Cloutier RR, Grodzinski B (2008) The iridoid glucoside, antirrhinoside, from Antirrhinum majus L. has differential effects on two generalist insect herbivores. J Chem Ecol 34:591–600

    Article  PubMed  CAS  Google Scholar 

  • Bidart-Bouzat MG, Imeh-Nathaniel A (2008) Global change effects on plant chemical defenses against insect herbivores. J Integr Plant Bio 50:1339–1354

    Article  CAS  Google Scholar 

  • Biere A, Marak HB, van Damme JMM (2004) Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140:430–441

    Article  PubMed  Google Scholar 

  • Binkley D, Vitousek PM (1987) Soil nutrient availability. In: Pearcy RW, Ehleringer JR, Mooney HA, Rundel RW (eds) Physiological plant ecology: field methods and instrumentation. Chapman and Hall, London, pp 75–96

    Google Scholar 

  • Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants—a hypothesis. J Ecol 83:887–889

    Article  Google Scholar 

  • Blumenthal DN (2005) Interrelated causes of plant invasion. Science 310:243–244

    Article  PubMed  CAS  Google Scholar 

  • Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–895

    Article  PubMed  Google Scholar 

  • Boros CA, Stermitz FR (1990) Iridoids. An Updated Review, Part I. J Nat Prod 53:1055–1147

    Article  CAS  Google Scholar 

  • Boros CA, Stermitz FR (1991) Iridoids. An Updated Review, Part 2. J Nat Prod 54:1173–1246

    Article  CAS  Google Scholar 

  • Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11

    Article  PubMed  Google Scholar 

  • Bowers MD (1984) Iridoid glycosides and host-plant specificity in larvae of the buckeye butterfly, Junonia coenia (Nymphalidae). J Chem Ecol 10:1567–1577

    Article  CAS  Google Scholar 

  • Bowers MD (1991) Iridoid glycosides. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 297–326

    Google Scholar 

  • Bowers MD, Puttick GM (1989) Iridoid glycosides and insect feeding preferences—gypsy moths (Lymantria dispar, Lymantriidae) and buckeyes (Junonia coenia, Nymphalidae). Ecol Entomol 14:247–256

    Article  Google Scholar 

  • Bowers MD, Stamp NE (1993) Effects of plant age, genotype, and herbivory on Plantago performance and chemistry. Ecology 74:1778–1791

    Article  Google Scholar 

  • Bowers MD, Collinge SK, Gamble SE, Schmitt J (1992) Effects of genotype, habitat, and seasonal variation on iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and the implications for insect herbivores. Oecologia 91:201–207

    Article  Google Scholar 

  • Bowman WD, Bahn L, Damm M (2003) Alpine landscape variation in foliar nitrogen and phosphorus concentrations and the relation to soil nitrogen and phosphorus availability. Arctic, Antarctic, and Alpine Research 35:144–149

    Article  Google Scholar 

  • Bryant JP, Chapin FS, Klein DR (1983) Carbon Nutrient Balance of Boreal Plants in Relation to Vertebrate Herbivory. Oikos 40:357–368

    Article  CAS  Google Scholar 

  • Burke IC, Lauenroth WK, Parton WJ (1997) Regional and temporal variation in net primary production and nitrogen mineralization in grasslands. Ecology 78:1330–1340

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

    Article  Google Scholar 

  • Cappuccino N, Arnason JT (2006) Novel chemistry of invasive exotic plants. Biol Lett 2:189–193

    Article  PubMed  CAS  Google Scholar 

  • Chapin FS III, Bloom AJ, Field CB, Waring RH (1987) Plant responses to multiple environmental factors. Bioscience 37:49–57

    Article  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS (1985) Resource Availability and Plant Antiherbivore Defense. Science 230:895–899

    Article  PubMed  CAS  Google Scholar 

  • Darrow K, Bowers MD (1999) Effects of herbivore damage and nutrient level on induction of iridoid glycosides in Plantago lanceolata. J Chem Ecol 25:1427–1440

    Article  CAS  Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534

    Article  Google Scholar 

  • El-Naggar LJ, Beal JL (1980) Iridoids. A Review. J Nat Prod 43:649–707

    Article  PubMed  CAS  Google Scholar 

  • Fajer ED, Bowers MD, Bazzaz FA (1992) The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in Plantago—a test of the carbon nutrient balance hypothesis. Am Nat 140:707–723

    Article  PubMed  CAS  Google Scholar 

  • Franzyk H, Jensen SR, Thale Z, Olsen CE (1999) Halohydrins and polyols derived from antirrhinoside: Structural revisions of muralioside and epimuralioside. J Nat Prod 62:275–278

    Article  PubMed  CAS  Google Scholar 

  • Fuchs A, Bowers MD (2004) Patterns of iridoid glycoside production and induction in Plantago lanceolata and the importance of plant age. J Chem Ecol 30:1723–1741

    Article  PubMed  CAS  Google Scholar 

  • Gardner DR, Stermitz FR (1988) Host plant utilization and iridoid glycoside sequestration by Euphydryas anicia (Lepidoptera, Nymphalidae). J Chem Ecol 14:2147–2168

    Article  CAS  Google Scholar 

  • Gowan E, Lewis BA, Turgeon R (1995) Phloem transport of antirrhinoside, an iridoid glycoside, in Asarina scandens (Scrophulariaceae). J Chem Ecol 21:1781–1788

    Article  CAS  Google Scholar 

  • Hamilton JG, Zangerl AR, Delucia EH, Berenbaum MR (2001) The carbon-nutrient balance hypothesis: its rise and fall. Ecol Lett 4:86–95

    Article  Google Scholar 

  • Handjieva NV, Ilieva EI, Spassov SL, Popov SS (1993) Iridoid glycosides from Linaria species. Tetrahedron 49:9261–9266

    Article  CAS  Google Scholar 

  • Harvey JA, Van Nouhuys S, Biere A (2005) Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids. J Chem Ecol 31:287–302

    Article  PubMed  CAS  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hierro JL, Callaway RM (2003) Allelopathy and exotic plant invasion. Plant Soil 256:29–39

    Article  CAS  Google Scholar 

  • Inderjit, Callaway RM, Vivanco JM (2006) Can plant biochemistry contribute to understanding of invasion ecology? Trends Plant Sci 11:574–580

    Article  PubMed  CAS  Google Scholar 

  • Jamieson MA, Bowers MD (2010) Iridoid glycoside variation in the invasive plant Dalmatian toadflax, Linaria dalmatica (Plantaginaceae), and sequestration by the biological control agent, Calophasia lunula. J Chem Ecol 36:70–79

    Article  PubMed  CAS  Google Scholar 

  • Jeanneret P, Schroeder C (1992) Biology and host specificity of Mecinus janthinus Germar (Col: Curculionidae), a candidate for the biological control of yellow and Dalmatian toadflax, Linaria vulgaris (L.) Mill. and Linaria dalmatica (L.) Mill. (Scrophulariaceae) in North American. Biocontrol Sci Technol 2:25–34

  • Karban R (2011) The ecology and evolution of induced resistance against herbivores. Funct Ecol 25:339–347

    Article  Google Scholar 

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

    Google Scholar 

  • Karban R, Myers JH (1989) Induced Plant-Responses to Herbivory. Annu Rev Ecol Syst 20:331–348

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 117:164–169

    Article  Google Scholar 

  • Klockars GK, Bowers MD, Cooney B (1993) Leaf variation in iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and oviposition of the Buckeye, Junonia coenia (Nymphalidae). Chemoecology 4:72–78

    Article  CAS  Google Scholar 

  • Koricheva J, Larsson S, Haukioja E, Keinanen M (1998) Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos 83:212–226

    Article  CAS  Google Scholar 

  • Logan BA, Demming-Adams B, Rosenstiel TN, Adams WW (1999) Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. Planta 209:213–220

    Article  PubMed  CAS  Google Scholar 

  • Marak HB, Biere A, van Damme JMM (2002) Two herbivore-deterrent iridoid glycosides reduce the in vitro growth of a specialist but not of a generalist pathogenic fungus of Plantago lanceolata L. Chemoecology 12:185–192

    Article  CAS  Google Scholar 

  • Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vazquez DP (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740

    Article  PubMed  Google Scholar 

  • Nieminen M, Suomi J, Van Nouhuys S, Sauri P, Riekkola ML (2003) Effect of iridoid glycoside content on oviposition host plant choice and parasitism in a specialist herbivore. J Chem Ecol 29:823–844

    Article  PubMed  CAS  Google Scholar 

  • Nykänen H, Koricheva J (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104:247–268

    Article  Google Scholar 

  • Orians CM, Ward D (2010) Evolution of plant defenses in nonindigenous environments. Annu Rev Entomol 55:439–459

    Article  PubMed  CAS  Google Scholar 

  • Pereyra PC, Bowers MD (1988) Iridoid glycosides as oviposition stimulants for the Buckeye butterfly, Junonia coenia (Nymphalidae). J Chem Ecol 14:917–928

    Article  CAS  Google Scholar 

  • Peterson RKD, Sing SE, Weaver DK (2005) Differential physiological responses of Dalmatian toadflax, Linaria dalmatica L. Miller, to injury from two insect biological control agents: Implications for decision-making in biological control. Environ Entomol 34:899–905

    Article  Google Scholar 

  • Prudic KL, Oliver JC, Bowers MD (2005) Soil nutrient effects on oviposition preference, larval performance, and chemical defense of a specialist insect herbivore. Oecologia 143:578–587

    Article  PubMed  Google Scholar 

  • Reudler Talsma JH, Biere A, Harvey JA, van Nouhuys S (2008) Oviposition cues for a specialist butterfly-plant chemistry and size. J Chem Ecol 34:1202–1212

    Article  PubMed  CAS  Google Scholar 

  • Saastamoinen M, van Nouhuys S, Nieminen M, O’Hara B, Suomi J (2007) Development and survival of a specialist herbivore, Melitaea cinxia, on host plants producing high and low concentrations of iridoid glycosides. Ann Zool Fenn 44:70–80

    Google Scholar 

  • Saner MA, Jeanneret P, Mullerscharer H (1994) Interaction among two biological control agents and the developmental stage of their target weed, Dalmatian Toadflax, Linaria dalmatica (L) Mill (Scrophulariaceae). Biocontrol Sci Techn 4:215–222

    Article  Google Scholar 

  • Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55

    Article  PubMed  Google Scholar 

  • Stamp N (2004) Can the growth-differentiation balance hypothesis be tested rigorously? Oikos 107:439–448

    Article  Google Scholar 

  • USDA, NRCS (2009a) The PLANTS Database. National Plant Data Center, Baton Rouge, LA 70874-4490 USA. Available online at http://plants.usda.gov (accessed June 2, 2009)

  • USDA, NRCS (2009b) Soil Survey Staff, Natural Resources Conservation Service, United States Department of Agriculture. Web Soil Survey. Available online at http://websoilsurvey.nrcs.usda.gov (accessed June 2, 2009)

  • Van Hezewijk BH, Bourchier RS, De Clerck-Floate RA (2010) Regional-scale impact of the weed biocontrol agent Mecinus janthinus on Dalmatian toadflax (Linaria dalmatica). Biol Control 55:197–202

    Article  Google Scholar 

  • Vujnovic K, Wein RW (1996) The biology of Canadian weeds. 106. Linaria dalmatica (L.) Mill. Can J Plant Sci 77:483–491

    Article  Google Scholar 

  • Ward SM, Fleischmann CE, Turner MF, Sing SE (2009) Hybridization between invasive populations of Dalmatian toadflax (Linaria genistifolia subsp. dalmatica) and yellow toadflax (Linaria vulgaris). Invasive Plant Science and Management. Invasive Plant Sci Management 2:369–378

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Wilson LM, Sing SE, Piper GL, Hansen RW, De Clerck-Floate R, MacKinnon DK, Randall C (2005) Biology and biological control of Dalmatian and yellow toadflax. USDA Forest Service, FHTET-05-13

  • Wurst S, Van Dam NM, Monroy F, Biere A, Van der Putten WH (2008) Intraspecific variation in plant defense alters effects of root herbivores on leaf chemistry and aboveground herbivore damage. J Chem Ecol 34:1360–1367

    Article  PubMed  CAS  Google Scholar 

  • Zangerl AR, Berenbaum MR (2005) Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore. P Natl Acad Sci-Biol 102:15529–15532

    Article  CAS  Google Scholar 

  • Zangerl AR, Berenbaum MR (2008) Selection for chemical trait remixing in an invasive weed after reassociation with a coevolved specialist. P Natl Acad Sci-Biol 105:4547–4552

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Many thanks to Sarah Travers, Patrick Travers, and Nicole Won for field and laboratory assistance. We also thank the City of Boulder, Boulder County, and Linda and Sergio Sanabria for use of their land to conduct research. Timothy Seastedt, William Bowman, Susan Beatty, and Yan Linhart provided helpful comments and feedback on drafts of this manuscript. And finally, we are appreciative of the thoughtful comments provided by two anonymous reviewers. Funding for this project was provided by Boulder County Open Space and Parks, the Department of Ecology and Evolutionary Biology at the University of Colorado, the Hazel Schmoll Research Fellowship in Colorado Botany, and National Science Foundation grants DEB 0614883 and 0808473.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mary A. Jamieson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jamieson, M.A., Bowers, M.D. Soil nitrogen availability and herbivore attack influence the chemical defenses of an invasive plant (Linaria dalmatica; Plantaginaceae). Chemoecology 22, 1–11 (2012). https://doi.org/10.1007/s00049-011-0087-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00049-011-0087-1

Keywords

Navigation