Skip to main content

Does Rust Infection of Willow Affect Feeding and Oviposition Behavior of Willow Leaf Beetles?

Abstract

Willows are often attacked by both herbivorous insects and rust fungi. Little is known about interactions between these two willow enemies. We studied whether feeding and oviposition behavior of the willow leaf beetle Plagiodera versicolora upon the willow hybrid Salix x cuspidata is affected when the rust fungus Melampsora allii-fragilis has attacked the plant. Laboratory bioassays revealed that adult willow leaf beetles significantly avoided feeding and oviposition on rust-infected leaves when compared to healthy leaves. Further bioassays aimed to elucidate the temporal and spatial scale of effects of rust infection on feeding behavior of adults. While infected parts of leaves were avoided at all times past infection tested (8, 12, and 16 days), symptom-free parts of infected leaves were only avoided 16 days past infection. Systemic effects extended only one leaf position up and two leaf positions down from the infection site.

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

References

  • Agrawal, A. A., Tuzun, S., and Bent, E. (eds.) (1999). Induced Plant Defences Against Pathogens and Herbivores, APS Press, St. Paul, Minnesota.

    Google Scholar 

  • Bach, C. E. (1994). Effects of herbivory and genotype on growth and survivorship of sand-dune willow (Salix cordata). Ecol. Entomol. 19: 303–309

    Google Scholar 

  • Bach, C. E. (2001). Long -term effects of insect herbivory on responses of Salix cordata to sand acretion. Ecology 82: 397–409.

    Google Scholar 

  • Bennett, R. N., and Wallsgrove, R. M. (1994). Secondary metabolites in plant defence mechanisms. New Phytol. 127: 617–633.

    CAS  Google Scholar 

  • Biswas, B. B., and Das, H. K. (1998). Plant-Microbe Interactions. Subcelluar Biochemistry, Vol. 29, Plenum, New York.

    Google Scholar 

  • Bostock, R. M., Karban, R., Thaler, J. S., Weymann, P. D., and Gilchrist, D. (2001). Signal interactions in induced resistance to pathogens and insect herbivores. Eur. J. Plant Pathol. 107: 103–111.

    Article  Google Scholar 

  • Brandenburger, W. (1985). Parasitische Pilze an Gefäß pflanzen in Europe, Fischer, Stuttgart, Germany.

    Google Scholar 

  • Chakravorty, A. K., and Scott, K. J. (1982). Biochemistry of host rust interactions. In Scott, K. J., and Chakravorty, A. K. (eds.), The Rust Fungi, Academic Press, London, pp. 179–222.

    Google Scholar 

  • Clausen, T., Bryant, J. P., Reichardt, P. B., and Werner, R. A. (1991). Long -term and short-term induction in quaking aspen: Related phenomena? In Tallamy, D. W., and Raupp, M. J. (eds.), Phytochemical Induction by Herbivores, Wiley, New York, pp. 71–84.

    Google Scholar 

  • Farrar, J. F. (1993). Sink strength and how do we measure it? Introduction. Plant Cell Environ. 16: 1015.

    Google Scholar 

  • Farrar, J. F., and Lewis, D. H. (1987). Nutrient relations in biotrophic infections. In Pegg, G. F., and Ayres, P. G. (eds.), Fungal Infection of Plants, Cambridge University Press, Cambridge, pp. 92–132.

    Google Scholar 

  • Felton, G. W., and Korth, K. L. (2000). Trade -offs between pathogen and herbivore resistance. Current Opin. Plant Biol. 3: 309–314.

    Article  Google Scholar 

  • Felton, G. W., Korth, K. L., Bi, J. L., Wesley, S. V., Huhman, D. V., Mathews, M. C., Murphy, J. B., Lamb, C., and Dixon, R. A. (1999). Inverse relationship between systemic resistance of plants to micoorganisms and to insect herbivory. Current Biol. 9: 317–320.

    Article  Google Scholar 

  • Friedli, J., and Bacher, S. (2001). Mutualistic interaction between a weevil and a rust fungus, two parasites of the weed Cirsium arvense. Oecologia 129: 571–576.

    Google Scholar 

  • Hakulinen, J. (1998). Nitrogen -induced reduction in leaf phenolic level is not accompanied by increased rust frequency in a compatible willow (Salix myrsinifolia)-Melampsora rust interaction. Physiol. Plant. 102: 101–110.

    Article  Google Scholar 

  • Hakulinen, J., and Julkunen-Tiitto, R. (2000). Variation in leaf phenolics of field-cultivated willow (Salix sp.) clones in relation to occurrence of Melampsora rust. Forest Pathol. 30: 29–41.

    Article  Google Scholar 

  • Hakulinen, J., Sorjonen, S., and Julkunen-Tiitto, R. (1999). Leaf phenolics of willow clones differing in resistance to Melampsora rust. Physiol. Plant. 105: 662–669.

    Article  Google Scholar 

  • Hallet, S. G., Paul, N. D., and Ayres, P. G. (1990). Botrytis cinerea kills groundsel (Senecio vulgaris) infected by rust (Puccinia lagenophorae). New Phytol. 114: 105–109.

    Google Scholar 

  • Hammerschmidt, R. (1999). Phytoalexins : What have we learned after 60 years? Annu. Rev. Phytopathol. 37: 285–306.

    Article  Google Scholar 

  • Hatcher, P. E. (1995). Three -way interactions between plant pathogenic fungi, herbivorous Insects and their host plants. Bid. Rev. 70: 639–694.

    Google Scholar 

  • Hatcher, P. E., and Paul, N. D. (2001). Plant, pathogen, herbivore interactions and their effects on weeds. In Jeger, M. J., and Spencer, N. J. (eds.), Biotic Interactions in Plant-Pathogen Associations, CAB International, Oxfordshire, pp. 193–225.

    Google Scholar 

  • Hatcher, P. E., Paul, N. D., Ayres, P. G., and Whittaker, J. B. (1994). The effect of a foliar disease (rust) on the development of Gastrophysa viridula (Coleoptera: Chrysomelidae). Ecol. Entomol. 19: 349–360.

    Google Scholar 

  • Hatcher, P. E., Paul, N. D., Ayres, P. G., and Whittaker, J. B. (1995). Interactions between Rumex spp., herbivores and a rust fungus: The effect of Uromyces rumicis infection on leaf nutritional quality. Funct. Ecol. 9: 97–105.

    Google Scholar 

  • Heath, M. C., and Skalamera, D. (1997). Cellular interactions between plants and parasites. Adv. Bot. Res. 24: 195–225.

    Google Scholar 

  • Heil, M. (2001). The ecological concept of costs of induced systemic resistance (ISR). Eur. J. Plant Pathol. 107: 137–146.

    Article  Google Scholar 

  • Ho, L. C. (1988). Metabolism and compartimentation of imported sugars in sink organs in relation to sink strength. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39: 355–378.

    Article  Google Scholar 

  • Honkanen, T., and Haukioja, E. (1998). Intra -plant regulation of growth and plant-herbivore interactions. Ecoscience 5: 470–479.

    Google Scholar 

  • Hsiao, T. H. (1985). Feeding behaviour. In Kerkut, G. A., and Gilbert, L. I. (eds.), Comprehensive Insect Physiology, Biochemistry and Pharmacology, Pergamon Press, Oxford, pp. 471–512.

    Google Scholar 

  • Hunter, M. D. (2000). Mixed signals and cross-talk: Interactions between plants, insects and plant pathogens. Agric. Forest Entomol. 2: 155–161.

    Article  Google Scholar 

  • Ikonen, A., Tahvanainen, J., and Roininen, H. (2001). Chlorogenic acid as an antiherbivore defence of willows against leaf beetles. Entomol. Exp. Appl. 99: 47–54.

    Google Scholar 

  • Julkunen-Tiitto, R., Hakulinen, J., and Meyer, B. (1994). The response of growth and secondary metabolism to Melampsora rusts in field cultivated willow (Salix) clones. Acta Horticult. 381: 679–682.

    Google Scholar 

  • Karban, R., and Baldwin, I. T. (1997). Induced Plant Responses to Herbivory, Chicago University Press, Chicago.

    Google Scholar 

  • Kok, L. T., Abad, R. G., and Baudoin, A. B. A. M. (1996). Effects of Puccinia carduorum on musk thistle herbivores. Biol. Control 6: 123–129.

    Article  Google Scholar 

  • Kolehmainen, J., Julkunen-Tiitto, R., Roininen, H., and Tahvanainen, J. (1995). Phenolic glucosides as feeding cues for willow-feeding leaf beetles. Entomol. Exp. Appl. 74: 235–243.

    Google Scholar 

  • Kombrink, E., and Schmelzer, E. (2001). The hypersensitive response and its role in local and systemic disease resistance. Eur. J. Plant Pathol. 107: 69–78.

    Article  Google Scholar 

  • Kombrink, E., and Somssich, I. E. (1995). Defence response of plants to pathogens. Adv. Bot. Res. 21: 1–33.

    Google Scholar 

  • Kúc, J. (1995). Phytoalexins, stress metabolism, and disease resistance in plants. Annu. Rev. Phytopathol. 33: 275–297.

    Article  Google Scholar 

  • Mendgen, K., Struck, C., Voegele, R. T., and Hahn, M. (2000). Biotrophy and rust haustoria. Physiol. Mol. Plant Pathol. 56: 141–145.

    Article  Google Scholar 

  • Moran, P. J. (1998). Plant -mediated interactions between insects and a fungal plant pathogen and the role of plant chemical responses to infection. Oecologia 115: 523–530.

    Article  Google Scholar 

  • Nuernberger, T. (1999). Signal perception in plant pathogen defense. Cell. Mol. Life Sci. 55: 167–182.

    Article  Google Scholar 

  • Orians, C. M., Huang, C. H., Wild, K. A., Dorfman, P., Zee, M. T. T., and Fritz, R. S. (1997). Willow hybridisation differentially affects preference and performance of herbivorous beetles. Entomol. Exp. Appl. 83: 285–294.

    Article  Google Scholar 

  • Packard, C. G., and Boardman, T. J. (1999). The use of percentages and size-specific indices to normalize physiological data for variation in body size: Wasted time, wasted effort? Comp. Biochem. Physiol. Part A 122: 37–44.

    Article  Google Scholar 

  • Paul, N. D., Hatcher, P. E., and Taylor, J. E. (2000). Coping with multiple enemies: An integration of molecular and ecological perspectives. Trends Plant Sci. 5: 220–225.

    Article  Google Scholar 

  • Pei, M. H., Hunter, T., and Ruiz, C. (1999). Occurrence of Melampsora rusts in biomass willow plantations for renewable energy in the United Kingdom. Biomass Bioenergy 17: 153–163.

    Article  Google Scholar 

  • Pei, M. H., Royle, D. J., and Hunter, T. (1996). Pathogenic specialization in Melampsora epitea var. epitea on Salix. Plant Pathol. 45: 679–690.

    Article  Google Scholar 

  • Raupp, M. J., and Sadof, C. S. (1989). Behavioural responses of a leaf beetle to injury-related changes in its salicaceous host. Oecologia 80: 154–157.

    Google Scholar 

  • Raupp, M. J., and Sadof, C. S. (1991). Responses of leaf beetles to injury-related changes in their salicaceous hosts. In Tallamy, D. W., and Raupp, M. J. (eds.), Phytochemical Induction by Herbivores, Wiley, New York, pp. 183–204.

    Google Scholar 

  • Rostás, M., and Hilker, M. (2002). Feeding damage by larvae of the mustard leaf beetle deters conspecific females from oviposition and feeding. Entomol. Exp. Appl. 103: 267–277.

    Article  Google Scholar 

  • Rostás, M., Simon, M., and Hilker, M. (2003). Ecological cross-effects of induced plant responses towards herbivores and phytopathogenic fungi. Basic Appl. Ecol. 4: 43–62.

    Google Scholar 

  • Rowell-Rahier, M., and Pasteels, J. M. (1990). Phenolglycosides and interactions at three trophic levels: Salicaceae-herbivores-predators. In Bernays, E. A. (ed.), Insect-Plant-Interactions, CRC Press, Boca Raton, pp. 75–94.

    Google Scholar 

  • Simon, M., and Hilker, M. (2003). Herbivores and pathogens on willow: Do they affect each other? Agric. Forest. Entomol. 5: 275–284.

    Article  Google Scholar 

  • Slusarenko, A. J., Fraser, R. S. S., and Van Loon, L. C. (2000). Mechanisms of Resistance to Plant Diseases, Kluwer Academic Press, Dordrecht.

    Google Scholar 

  • Staples, R. C. (2000). Research on the rust fungi during the twentieth century. Annu. Rev. Phytopathol. 38: 49–69.

    Article  Google Scholar 

  • Sticher, L., Mauch-Mani, B., and Métraux, J. P. (1997). Systemic acquired resistance. Annu. Rev. Phytopathol. 35: 235–270.

    Article  Google Scholar 

  • Stout, M. J., Fidantsef, A. L., Duffey, S. S., and Bostock, R. M. (1999). Signal interactions in pathogen and insect attack: Systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum. Physiol. Mol. Plant Pathol. 54: 115–130.

    Article  Google Scholar 

  • Tahvanainen, J., Julkunen-Tiitto, R., and Kettunen, J. (1985). Phenolic glycosides govern the food selection pattern of willow feeding leaf beetles. Oecologia 67: 52–56.

    Article  Google Scholar 

  • Wagner, S., and Boyle, C. (1995). Changes in carbohydrate, protein and chlorophyll content, and enzyme activity during the switch from uredinio- to teliospore sporulation in the bean-rust fungus Uromyces appendiculatus (Pers.) Link. J. Phytopathol. 143: 633–638.

    Google Scholar 

  • Wardlaw, I. F. (1990). The control of carbon partitioning in plant. New Phytol. 116: 341–381.

    CAS  Google Scholar 

  • Zulu, J. N., Farrar, J. F., and Whitbread, R. (1991). Effects of phosphate supply on wheat seedlings infected with powdery mildew: Carbohydrate metabolism of first leaves. New Phytol. 118: 553–558.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Monika Hilker.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Simon, M., Hilker, M. Does Rust Infection of Willow Affect Feeding and Oviposition Behavior of Willow Leaf Beetles?. J Insect Behav 18, 115–129 (2005). https://doi.org/10.1007/s10905-005-9351-y

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10905-005-9351-y

  • Plagiodera
  • Chrysomelidae
  • Salix
  • phytopathogen
  • Melampsora
  • food consumption
  • oviposition