Skip to main content
Log in

Induced defense in Nicotiana attenuata (Solanaceae) fruit and flowers

  • Plant Animal Interactions
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Plants protect themselves against herbivory using a continuum of strategies, ranging from constitutive defenses to intermittent induced responses. Induced defenses may not provide immediate and maximum protection, but could be advantageous when continuous defense is either energetically or ecologically costly. As such, induced defenses in flowers could help defend relatively valuable tissue while keeping reproductive structures accessible and attractive to pollinators. Thus far, no one has demonstrated the efficacy of induced defenses against floral herbivores (florivores) in the field. Here we show that mechanical leaf damage in wild tobacco, Nicotiana attenuata (Solanaceae), reduced both flower and fruit herbivory in the field and that exogenous application of methyl jasmonate, a potent elicitor of induced responses, reduced both leaf and floral damage in natural populations. This result is consistent with a survey of damage in the field, which showed a negative relationship between leaf damage and flower and fruit damage. Although optimal defense theory predicts that induced defenses should be rare in reproductive tissues, owing to their high fitness value, our results suggest otherwise. Induced defenses in leaves and reproductive tissues may allow plants to respond effectively to the concomitant pressures of defending against herbivory and attracting pollinators.

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

Similar content being viewed by others

References

  • Agrawal AA (2001) Transgenerational consequences of plant responses to herbivory: an adaptive maternal effect? Am Nat 157:555–569

    Article  CAS  PubMed  Google Scholar 

  • Agrawal AA, Strauss SY, Stout MJ (1999) Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53:1093–1104

    Article  Google Scholar 

  • Aigner PA, Scott PE (2002) Use and pollination of a hawkmoth plant, Nicotiana attenuata, by migrant hummingbirds. Southwest Nat 47:1–11

    Article  Google Scholar 

  • Baldwin IT (1988) The alkaloidal responses of wild tobacco to real and simulated herbivory. Oecologia 77:378–381

    Article  Google Scholar 

  • Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci USA 95:8113–8118

    Article  PubMed  CAS  Google Scholar 

  • Baldwin IT, Karb MJ (1995) Plasticity in allocation of nicotine to reproductive parts in Nicotiana attenuata. J Chem Ecol 21:897–909

    Article  CAS  Google Scholar 

  • Breadmore KN, Kirk WDJ (1998) Factors affecting floral herbivory in a limestone grassland. Acta Oecol 19:501–506

    Article  Google Scholar 

  • Conover WJ, Iman RI (1981) Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 35:124–129

    Article  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381

    Article  PubMed  CAS  Google Scholar 

  • Euler M, Baldwin IT (1996) The chemistry of defense and apparency in the corollas of Nicotiana attenuata. Oecologia 107:102–112

    Article  Google Scholar 

  • Fenster CB, Galloway LF (2000) Inbreeding and outbreeding depression in natural populations of Chamaecrista fasciculata (Fabaceae). Conserv Biol 14:1406–1412

    Article  Google Scholar 

  • Fineblum WL, Rausher MD (1997) Do floral pigmentation genes also influence resistance to enemies? The W locus in Ipomoea purpurea. Ecology 78:1646–1654

    Google Scholar 

  • Gronquist M, Bezzerides A, Attygalle A, Meinwald J, Eisner M, Eisner T (2001) Attractive and defensive functions of the ultraviolet pigments of a flower (Hypericum calycinum). Proc Natl Acad Sci USA 98:13745–13750

    Article  PubMed  CAS  Google Scholar 

  • Irwin RE, Strauss SY, Storz S, Emerson A, Guibert G (2003) The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84:1733–1743

    Article  Google Scholar 

  • Irwin RE, Adler LS (2005) Correlations among traits associated with herbivore resistance and pollination: implications for pollination and nectar robbing in a distylous plant. Am J Bot 93(1) (in press)

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

    Google Scholar 

  • Karban R, Strauss SY (1993) Effects of herbivores on growth and reproduction of their perennial host, Erigeron glaucus. Ecology 74:39–46

    Article  Google Scholar 

  • Karban R, Maron J, Felton GW, Ervin G, Eichenseer H (2003) Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants. Oikos 100:325–332

    Article  Google Scholar 

  • Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328

    Article  PubMed  CAS  Google Scholar 

  • Krupnick GA, Weis AE (1999) The effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80:135–149

    Google Scholar 

  • Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161

    Article  Google Scholar 

  • McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320

    Article  Google Scholar 

  • Neter J, Kutner MH, Wasserman W, Nachtsheim CJ (1996) Appied linear statistical models, 4th edn. McGraw-Hill, Irwin

    Google Scholar 

  • Reinbothe S, Mollenhauer B, Reinbothe C (1994) Jips and rips: the regulation of plant gene expression by jasmonates in response to environmental cues and pathogens. Plant Cell 6:1197–1209

    Article  PubMed  CAS  Google Scholar 

  • Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–719

    Article  PubMed  CAS  Google Scholar 

  • Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites, 1st edn. Academic, New York

    Google Scholar 

  • Rhoades DF, Cates RG (1976) Toward a general theory of plant antiherbivore chemistry. Recent Adv Phytochem 10:168–210

    CAS  Google Scholar 

  • Schaller F (2001) Enzymes of the biosynthesis of octadecanoid-derived signalling molecules. J Exp Bot 52:11–23

    Article  PubMed  CAS  Google Scholar 

  • Scheiner SM (2001) MANOVA: multiple response variables and multispecies interactions. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 99–115

    Google Scholar 

  • Strauss SY (1997) Floral characters link herbivores, pollinators, and plant fitness. Ecology 78:1640–1645

    Article  Google Scholar 

  • Strauss SY, Irwin RE, Lambrix VM (2004) Optimal defence theory and flower petal colour predict variation in secondary chemistry of wild radish. J Ecol 92:132–141

    Article  Google Scholar 

  • Wells PV (1959) An ecological investigation of two desert tobaccos. Ecology 40:626–644

    Article  Google Scholar 

  • Zangerl AR, Berenbaum MR (1993) Plant chemistry, insect adaptations to plant chemistry, and host plant utilization patterns. Ecology 74:47–54

    Article  CAS  Google Scholar 

  • Zangerl AR, Rutledge CE (1996) The probability of attack and patterns of constitutive defense: a test of optimal defence theory. Am Nat 147:599–608

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dan Dawson for allowing the use of SNARL facilities and property for our experiments. Mikaela Huntzinger, Rebecca Balogh, and Sarah Elmendorf all helped with field work. Comments on this manuscript were contributed by Lynn Adler, Judie Bronstein, Jay Rosenheim, Sharon Strauss, and two anonymous reviewers. We thank Lynn Adler and Rebecca Irwin for access to unpublished works. A.M. was supported with a Ford Foundation Predoctoral Grant, a UC-Davis Jastro-Shields award, a University of California NRS Mathias Grant, the UC-Davis Entomology Department, and the UC-Davis Center for Population Biology. R.K. was supported by an NSF grant # DEB 0121050. We also thank the UC-Davis Plant-Insect group for stimulating comments during the project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrew C. McCall.

Additional information

Communicated by Jim Ehleringer

Rights and permissions

Reprints and permissions

About this article

Cite this article

McCall, A.C., Karban, R. Induced defense in Nicotiana attenuata (Solanaceae) fruit and flowers. Oecologia 146, 566–571 (2006). https://doi.org/10.1007/s00442-005-0284-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-005-0284-0

Keywords

Navigation