Skip to main content
SpringerLink
Log in

Effects of Simulated Herbivory on Defensive Compounds in Forage Plants of Norwegian Alpine Rangelands

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

A field study on the effects of current grazing practices on plants in central Norway found no increase in either phenolic compounds or proteinase inhibitors in plants subjected to grazing by sheep. This could either reflect insufficient damage to the plants due to low grazing intensity or a lack of a long-term response of the plants to grazing. In this study, we tested the hypothesis that damage to forage plants used by sheep and rodents in Norwegian alpine rangelands can stimulate a long-term (at least 2-week) increase in levels of defensive compounds. We used clipping experiments to manipulate the severity and timing of damage to eight species of common plants used by herbivores in Norway. Under greenhouse conditions (i.e., climate-controlled), we subjected mature plants to one of four clipping treatments: control (0% leaf tissue removed), low (10–15% leaf tissue removed), high (70–75% leaf tissue removed), or sustained (15% of leaf tissue removed every other day up to a total removal of 75%, i.e., five clippings over 9 days). Samples were collected 2 weeks after final clipping and analyzed for concentrations of total phenolics, proteinase inhibitors, ratio of total phenolics to soluble proteins, and ratio of proteinase inhibitors to soluble plant proteins. As expected, the different species of plants responded differently to simulated herbivory, but most plants either showed no response to mechanical wounding and tissue loss or had reduced defensive compounds. Thus, our results do not support the hypothesis that herbivory induces a long-term increase in defensive compounds in alpine rangelands of Norway, a result consistent with those from field studies.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Adler, F. R. and Karban, R. 1994. Defended fortresses or moving targets? Another model of inducible defenses inspired by military metaphors. Am. Nat. 144:813-832.

    Article  Google Scholar 

  • Agrawal, A. A. 1998. Induced responses to herbivory and increased plant performance. Science 279:1201-1202.

    Article  PubMed  Google Scholar 

  • Åström, M. and Lundberg, P. 1994. Plant defense and stochastic risk of herbivory. Evol. Ecol. 8:288-298.

    Article  Google Scholar 

  • Baldwin, I. T. 1990. Herbivory simulations in ecological research. Tree 5:91-93.

    Google Scholar 

  • Baldwin, I. T. 1988. The alkaloidal responses of wild tobacco to real and simulated herbivory. Oecologia 77:378-381.

    Article  Google Scholar 

  • Bazely, D. R., Vicari, M., Emmerich, S., Filip, L., Lin, D., and Inman, A. 1997. Interactions between herbivores and endophyte-infected Festuca rubra from the Scottish islands of St. Kilda, Benbeula and Rum. J. Appl. Ecol. 34:847-860.

    Article  Google Scholar 

  • Bergmeyer, H. U. and Gawehn, K. 1974. Methods of Enzymatic Analysis. Academic, New York

    Google Scholar 

  • Bradford, M. M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.

    Article  PubMed  Google Scholar 

  • Bråthen, K. A., Agrell, J., Berteaux, D., and Jonsdottir, I. S. 2004. Intraclonal variation in defense substances and palatability: a study on Carex and lemmings. Oikos 105:461-470.

    Article  Google Scholar 

  • Britton, A. J., Pearce, I. S. K., and Jones, B. 2005. Impacts of grazing on montane heath vegetation in Wales and implications for the restoration of montane areas. Biol. Conserv. 125:515-524.

    Article  Google Scholar 

  • Brown, D. G., and Weis, A. E. 1995. Direct and indirect effects of prior grazing of goldenrod upon the performance of a leaf beetle. Ecology 76:426-436.

    Article  Google Scholar 

  • Bryant, J. P., Wieland, G. D., Clausen, T., and Kuropat, P. 1985. Interactions of snowshoe hare and feltleaf willow in Alaska. Ecology 66:1564-1573.

    Article  Google Scholar 

  • Cates, R. G. 1975. The interface between slugs and wild ginger: some evolutionary aspects. Ecology 56:391-400.

    Article  Google Scholar 

  • Cipollini, D. F., and Bergelson, J. 2000. Environmental and developmental regulation of trypsin inhibitor activity in Brassica napus. J. Chem. Ecol. 26:1411-1422.

    Article  Google Scholar 

  • Cipollini, D. F. and Sipe, M. L. 2001. Jasmonic acid treatment and mammalian herbivory differentially affect chemical defenses and growth of wild mustard (Brassica caber). Chemoecology 11:137-143.

    Article  Google Scholar 

  • Coleman, R. A., Ramchunder, S. J., Moody, A. J., and Foggo, A. 2007. An enzyme in snail saliva induces herbivore-resistance in a marine alga. Funct. Ecol. 21:101-106.

    Article  Google Scholar 

  • Crawley, M. J. 1999. Herbivory, pp 199-217, in M. C. Press, J. D. Scholes, and M. G. Barker (eds.). Physiological Plant Ecology. Blackwell Science, Oxford.

    Google Scholar 

  • Donaldson, J. R., Kruger, E. L., and Lindroth, R. L. 2005. Competition- and resource-mediated tradeoffs between growth and defensive chemistry in trembling aspen (Populus tremuloides). New Phytol. 169:561-570.

    Article  Google Scholar 

  • Estell, R. E., Fredrickson, E. L., Anderson, D. M., Havstad, K. M., and Remmenga, M. D. 1998. Relationship of tarbush leaf surface terpene profile with livestock herbivory. J. Chem. Ecol. 24:1-12.

    Article  Google Scholar 

  • Faeth, S. H. 1986. Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67:479-494.

    Article  Google Scholar 

  • Green, T. R., and Ryan, C. A. 1972. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776-777.

    Article  PubMed  Google Scholar 

  • Gustafson, G. and Ryan, C. A. 1976. Specificity of protein turnover in tomato leaves -- accumulation of proteinase inhibitors, induced with wound hormone, PIIf. J Biol Chem. 251:7004-7010.

    PubMed  Google Scholar 

  • Hambäck, P. A., Grellmann, D., and Hjältén, J. 2002. Winter herbivory by voles during a population peak: the importance of plant quality. Ecography 25:74-80.

    Article  Google Scholar 

  • Harborne, J. B. 1991. The chemical basis of plant defense, pp. 45-59, in R. T. Palo and C. T. Robbins (eds.). Plant Defenses Against Mammalian Herbivory. CRC, Boca Raton.

    Google Scholar 

  • Hartley, S. E., and Lawton, J. H. 1987. Effects of different types of damage on the chemistry of birch foliage, and the responses of birch feeding insects. Oecologia 74:432-437.

    Article  Google Scholar 

  • Haukioja, E., and Neuvonen, S. 1985. Induced long-term resistance of birch foliage against defoliators: defensive or incidental? Ecology 66:1303-1308.

    Article  Google Scholar 

  • Högstedt, G., and Seldal, T. 1998. Sauebeiting i fjellet. Bruk og forvaltning av utmark. Seminar held 4.-5. March 1998: Norges Forskningsråd.

  • Karban, R. 1986. Induced resistance against spider mites in cotton: field verification. Entomol. Exp. Appl. 42:239-242.

    Article  Google Scholar 

  • Kausrud, K., Mysterud, A., Rekdal, Y., Holand, Ø., and Austrheim, G. 2006. Density-dependent foraging behaviour of sheep on alpine pastures: effects of scale. J. Zool. 270:63-71.

    Google Scholar 

  • Kavitha, R., and Umesha, S. 2008. Regulation of defense-related enzymes associated with bacterial spot resistance in tomato. Phytoparasitica 36:144-159.

    Article  Google Scholar 

  • Lindgren, Å., Klint, J., and Moen, J. 2007. Defense mechanisms against grazing: a study of trypsin inhibitor responses to simulated grazing in the sedge Carex bigelowii. Oikos 116:1540-1546.

    Article  Google Scholar 

  • Massey, F. P., and Hartley, S. E. 2006. Experimental demonstration of the antiherbivore effects of silica in grasses: impacts on foliage digestibility and vole growth rates. Proc. R. Soc. Lond. B Biol. Sci. 273:2299-2304.

    Article  Google Scholar 

  • Massey, F. P., Ennos, A. R., and Hartley, S. E. 2007. Herbivore specific induction of silica-based plant defenses. Oecologia 152:677-683.

    Article  PubMed  Google Scholar 

  • Müller-schwarze, D., and Thoss, V. 2008. Defense on the rocks: Low monoterpenoid levels in plants on pillars without mammalian herbivores. J. Chem. Ecol. 34:1377-1381.

    Article  PubMed  Google Scholar 

  • Mysterud, I., and Warren, J. T. 1991. Sau og barskogsforvaltning. Fauna 44:41-61.

    Google Scholar 

  • Mysterud, A., and Mysterud, I. 2000. Økologiske effekter av husdyrbeiting i utmark: III. Påvirkning på mindre pattedyr, fugler og virvelløse dyr. Fauna 53:106-116.

    Google Scholar 

  • Mysterud, A., and Austrheim, G. 2005. Økologiske effekter av sauebeiting i høyfjellet: Korttidseffekter. Utmarksnæring i Norge no. 1-05.

  • Neuvonen, S., Haukioja, E., and Molarius, A. 1987. Delayed inducible resistance against a leaf-chewing insect in four deciduous tree species. Oecologia 74:363-369.

    Article  Google Scholar 

  • Oksanen, L., Oksanen, T., Lukkari, A., and Siren, S. 1987. The role of phenol-based inducible defense in the interaction between tundra populations of the vole Clethrionomys rufocanus and the dward shrub Vaccinium myrtillus. Oikos 50:371-380.

    Article  Google Scholar 

  • Pontoppidan, B., Hopkins, R., Rask, L., and Meijer, J. 2005. Differential wound induction of the myrosinase system in oilseed rape (Brassica napus): contrasting insect damage with mechanical damage. Plant Sci. 168:715-722.

    Article  Google Scholar 

  • Redak, R. A., and Capinera, J. L. 1994. Changes in western wheatgrass foliage quality following defoliation: consequences for a graminivorous grasshopper. Oecologia 100:80-88.

    Article  Google Scholar 

  • Rosenthal, G, A., and Berenbaum, M. R. 1991. Herbivores: Their Interaction with Secondary Plant Metabolites (2nd ed.). Volume I: The Chemical Participants. Academic, New York.

    Google Scholar 

  • Saetnan, E. R. 2008. Interaction of arvicoline rodents and sheep in Norwegian alpine rangeland. Ph.D. dissertation, University of Illinois at Urbana–Champaign, USA.

  • Saetnan, E. R., Gjersvold, J. O., and Batzli, G. O. 2009. Habitat use and diet composition of Norwegian lemmings and field voles in central Norway. J. Mammal. 90:183-188.

    Article  Google Scholar 

  • Scheiner, S. M. 2001. Multiple response variables and multi-species interactions, pp. 99-115, in S. M. Scheiner and J. Gurevitch (eds.) Design and Analysis of Ecological Experiments. 2nd edition. Chapman and Hall, New York.

    Google Scholar 

  • Seldal, T., Andersen, K.-J., and Högstedt, G. 1994. Grazing-induced proteinase inhibitors: a possible cause for lemming population cycles. Oikos 70:3-11.

    Article  Google Scholar 

  • Singleton, V. L., Orthofer, R., and Lamuela-Raventos, R. M. 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 299:152-178.

    Article  Google Scholar 

  • Strengbom, J., Olofsson, J., Witzell, J., and Dahlgren, J. 2003. Effects of repeated damage and fertilization on palatability of Vaccinium myrtillus to grey sided voles, Clethrionomys rufocanus. Oikos 103:133-141.

    Article  Google Scholar 

  • Zangerl, A. R., Arntz, A. M., and Berenbaum, M. R. 1997. Physiological price of an induced chemical defense: photosynthesis, respiration, biosynthesis, and growth. Oecologia 109:433-441.

    Article  Google Scholar 

Download references

Acknowledgments

Financial support for this project was provided by the Program for Ecology and Evolutionary Biology at the University of Illinois at Urbana–Champaign. All chemical analyses were completed at the University of Essex with the help of Richard Webster.

Author information

Authors and Affiliations

  1. Program for Ecology and Evolutionary Biology, Department of Animal Biology, University of Illinois at Urbana–Champaign, 505 S. Goodwin Avenue, Urbana, IL, 61801, USA

    Eli R. Saetnan & George O. Batzli

  2. Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Penglais, Aberystwyth, Ceredigion, SY23 3DA, UK

    Eli R. Saetnan

Authors
  1. Eli R. Saetnan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. George O. Batzli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eli R. Saetnan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saetnan, E.R., Batzli, G.O. Effects of Simulated Herbivory on Defensive Compounds in Forage Plants of Norwegian Alpine Rangelands. J Chem Ecol 35, 469–475 (2009). https://doi.org/10.1007/s10886-009-9616-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-009-9616-6

Keywords

Search

Navigation