Skip to main content
Log in

Effects of elevated ultraviolet-B radiation on a plant–herbivore interaction

  • Plant-Animal interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Enhanced ultraviolet-B (UV-B) radiation may have multiple effects on both plants and animals and affect plant–herbivore interactions directly and indirectly by inducing changes in host plant quality. In this study, we examined combined effects of UV-B and herbivory on the defence of the mountain birch (Betula pubescens ssp. czerepanovii) and also the effects of enhanced UV-B radiation on a geometrid with an outbreak cycle: the autumnal moth (Epirrita autumnata). We established an experiment mimicking ozone depletion of 30% (a relevant level when simulating ozone depletion above Northern Lapland). Both arctic species responded only slightly to the enhanced level of UV-B radiation, which may indicate that these species are already adapted to a broader range of UV-B radiation. UV-B exposure slightly induced the accumulation of myricetin glycosides but had no significant effect on the contents of quercetin or kaempferol derivatives. Mountain birch seedlings responded more efficiently to herbivory wounding than to enhanced UV-B exposure. Herbivory induced the activities of foliar oxidases that had earlier been shown to impair both feeding and growth of moth larvae. In contrast, the contents of foliar phenolics did not show the same response in different clones, except for a decrease in the contents of tannin precursors. The induction of foliar phenoloxidase activities is a specific defence response of mountain birches against insect herbivory. To conclude, our results do not support the hypothesis that the outbreak cycle of the autumnal moth can be explained by the cycles of solar activity and UV-B.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511–1530

    Article  CAS  PubMed  Google Scholar 

  • Bi JL, Murphy JB, Felton GW (1997) Antinutritive and oxidative components as mechanisms of induced resistance in cotton to Helicoverpa zea. J Chem Ecol 23:97–117

    Article  CAS  Google Scholar 

  • Björn LO (1990) Practical hints for the UV-B photobiologist. Photobiology, 2nd edn. University of Lund, Lund

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Buck N, Callaghan TV (1999) The direct and indirect effects of enhanced UV-B on the moth caterpillar Epirrita autumnata. Ecol Bull 47:68–76

    Google Scholar 

  • Caldwell MM, Ballaré CL, Bornman JF, Flint SD, Björn LO, Teramura AH, Kulandaivelu G, Tevini M (2003) Terrestrial ecosystems, increased solar ultraviolet radiation and interactions with other climatic change factors. Photochem Photobiol Sci 1:29–38

    Article  Google Scholar 

  • Chan T, Galati G, O’Brien PJ (1999) Oxygen activation during peroxidase catalysed metabolism of flavones or flavanones. Chem Biol Interact 122:15–25

    Article  CAS  PubMed  Google Scholar 

  • Constabel CP, Yip L, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol 124:285–295

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Farman JC, Gardiner BG, Shanklin JD (1985) Large losses of total ozone in Antarctica reveal seasonal CLOx/NOx interaction. Nature 315:207–210

    Article  CAS  Google Scholar 

  • Felton GW, Donato K, Del Vecchio RJ, Duffey SS (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J Chem Ecol 15:2667–2694

    Article  CAS  PubMed  Google Scholar 

  • Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643

    Article  CAS  PubMed  Google Scholar 

  • Grassmann J, Hippeli S, Elstner EF (2002) Plant defence and its benefits for animals and medicine: role of phenolics and terpenoids in avoiding oxygen stress. Plant Physiol Biochem 40:471–478

    Article  CAS  Google Scholar 

  • Gwynn-Jones D (1999) Enhanced UV-B radiation and herbivory. Ecol Bull 47:77–83

    Google Scholar 

  • Haruta M, Pedersen JA, Constabel CP (2001) Polyphenol oxidase and herbivore defense in trempling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol Plant 112:552–558

    Article  CAS  PubMed  Google Scholar 

  • Haukioja E (2003) Putting the insects into the birch–insect interaction. Oecologia 136:161–168

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Haukioja E, Niemelä P (1979) Birch leaves as a resource for herbivores: seasonal occurrence of increased resistance in foliage after mechanical damage. Oecologia 39:151–159

    Article  Google Scholar 

  • Izaguirre MM, Mazza CA, Svatos A, Baldwin IT, Ballare CL (2007) Solar ultarviole-B radiation and insect herbivory trigger partially overlapping phenolic response in Nicotiana attenuata and Nicotiana longiflora. Ann Bot 99:103–109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Julkunen-Tiitto R, Sorsa S (2001) Testing the effects of drying methods on willow flavonoids, tannins, and salicylates. J Chem Ecol 27:779–789

    Article  CAS  PubMed  Google Scholar 

  • Julkunen-Tiitto R, Häggman H, Aphalo PJ, Lavola A, Tegelberg R, Veteli T (2005) Growth and defense in deciduous trees and shrubs under UV-B. Environ Poll 137:404–414

    Article  CAS  Google Scholar 

  • Kaitaniemi P, Ruohomäki K (2001) Sources of variability in plant resistance against insects: free caterpillars show strangest effects. Oikos 95:461–470

    Article  Google Scholar 

  • Kapari L, Haukioja E, Rantala MJ, Ruuhola T (2006) Immune defence of a defoliating insect interacts with induced plant defence during a population outbreak. Ecology 87:291–296

    Article  PubMed  Google Scholar 

  • Karabourniotis G, Kyparissis A, Manetas Y (1993) Leaf hairs of Olea europaea protect underlying tissue against ultraviolet-B radiation damage. Environ Bot 33:341–345

    Article  Google Scholar 

  • Keski-Saari S, Pusenius J, Julkunen-Tiitto R (2005) Phenolic compounds in seedlings of Betula pubescens and B. pendula are affected by enhanced UVB radiation and different nitrogen regimens during early ontogeny. Glob Change Biol 11:1180–1194

    Article  Google Scholar 

  • Kinnunen H, Huttunen S, Laakso K (2001) UV-absorbing compounds and waxes of Scots pine needles during a third growing season of supplemental UV-B. Environ Poll 112:215–220

    Article  CAS  Google Scholar 

  • Klemola N, Klemola T, Rantala M, Ruuhola T (2007) Natural host plant quality affects immune defence of the insect herbivore. Entomol Exp Appl 123:167–176

    Article  CAS  Google Scholar 

  • Lavola A, Julkunen-Tiitto R, Roininen H, Aphalo P (1998) Host-Plant preference of an insect herbivore mediated by UV-B and CO2 in relation to plant secondary metabolites. Biochem Syst Ecol 26:1–12

    Article  CAS  Google Scholar 

  • Lindroth RL, Peterson SS (1988) Effects of plant phenols on performance of southern armyworm larvae. Oecologia 75:185–189

    Article  Google Scholar 

  • Lindroth RL, Hofmann RW, Campbell BD, McNabb WC, Hunt DY (2000) Population differences in Trifolium repens L. response to ultraviolet-B radiation: foliar chemistry and consequences for two Lepidopteran herbivores. Oecologia 122:20–28

    Article  Google Scholar 

  • Madronich S, McKenzie RL, Björn LO, Caldwell MM (1998) Changes in biologically active ultraviolet radiation reaching the Earth’s surface. J Photochem Photobiol B 46:5–19

    Article  CAS  PubMed  Google Scholar 

  • Mazza CA, Zavala J, Scopel AL, Ballaré CL (1999) Perception of solar UVB radiation by phytophagous insects: behavioral responses and ecosystem implications. Proc Natl Acad Sci USA 96:980–985

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McCloud ES, Berenbaum MR, Tuveson RW (1992) Furanocoumarin content and phototoxicity of rough lemon (Citrus jambhiri) foliage exposed to enhanced ultraviolet-B (UVB) irradiation. J Chem Ecol 18:1125–1137

    Article  CAS  PubMed  Google Scholar 

  • Nappi AJ, Ottaviani E (2000) Cytotoxicity and cytotoxic molecules in invertebrates. Bioassays 22:469–480

    Article  CAS  Google Scholar 

  • Nappi AJ, Vass E, Frey F, Carton Y (1995) Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. Eur J Cell Biol 68:450–456

    CAS  PubMed  Google Scholar 

  • Nilssen AC, Tenow O, Bylund H (2007) Waves and synchrony in Epirrita autumnata/Operophtera brumata outbreaks. II. Sunspot activity cannot explain cyclic outbreaks. J Anim Ecol 76:269–275

    Article  CAS  PubMed  Google Scholar 

  • Nurmi K, Ossipov V, Haukioja E, Pihlaja K (1996) Variation of total phenolic content and individual low-molecular weight phenolics in foliage of mountain birch trees. J Chem Ecol 22:2023–2040

    Article  CAS  PubMed  Google Scholar 

  • Olsson LC, Veit M, Weissenböck G, Bornman JF (1998) Differential flavonoid response to enhanced UV-B radiation in Brassica napus. Phytochemistry 49:1021–1028

    Article  CAS  Google Scholar 

  • Paul ND, Gwynn-Jones D (2003) Ecological roles of solar UV radiation: towards an integrated approach. Trends Ecol Evol 18:48–55

    Article  Google Scholar 

  • Paul ND, Rasanayagam S, Moody SA, Hatcher PE, Ayres PG (1997) The role of interactions between trophic levels in determining the effects of UV-B on terrestrial ecosystems. Plant Ecol 128:296–308

    Article  Google Scholar 

  • Rantala MJ, Kortet R (2003) Courtship song and immune function in the field cricket Gryllus bimaculatus? Biol J Linn Soc 79:503–510

    Article  Google Scholar 

  • Rantala MJ, Roff DA (2007) Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata. Heredity 98:329–336

    Article  CAS  PubMed  Google Scholar 

  • Rice-Evans CA, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2:152–159

    Article  Google Scholar 

  • Ruohomäki K, Tanhuanpää M, Ayres MP, Kaitaniemi P, Tammaru T, Haukioja E (2000) Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice. Popul Ecol 42:211–223

    Article  Google Scholar 

  • Ruuhola T, Yang S (2006) Wound-induced oxidative responses in mountain birch leaves. Ann Bot 97:29–37

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ruuhola T, Tikkanen O-P, Tahvanainen J (2001) Differences in host use efficiency of larvae of a generalist moth, Operopthera brumata on three chemically divergent Salix species. J Chem Ecol 27:1595–1615

    Article  CAS  PubMed  Google Scholar 

  • Ruuhola T, Salminen J-P, Haviola S, Yang S, Rantala MJ (2007) Immunological memory of mountain birches: effects of phenolics on performance of the autumnal moth depend on herbivory history of trees. J Chem Ecol 33:1160–1176

    Article  CAS  PubMed  Google Scholar 

  • Ruuhola T, Yang S, Ossipov V, Haukioja E (2008) Foliar oxidases as mediators of the rapidly induced resistance of mountain birch against Epirrita autumnata. Oecologia 154:725–730

    Article  PubMed  Google Scholar 

  • Ryan KG, Markham KR, Bloor SJ, Bradley J m, Mitchell KA, Jordan BR (1998) UV-B radiation induced increase in quercetin:kaempferol ratio in normal and transgenic lines of Petunia. Photochem Photobiol 68:323–330

    CAS  Google Scholar 

  • Selås V, Hogstad A, Kobro S, Rafoss T (2004) Can sunspot activity and ultraviolet-B radiation explain cyclic outbreaks of forest moth pest species? Proc Biol Sci 271:1897–1901

    Article  PubMed Central  PubMed  Google Scholar 

  • Tahvanainen J, Julkunen-Tiitto R, Kettunen J (1985) Phenolic glycosides govern the food selection pattern of willow feeding leaf beetles. Oecologia 65:319–323

    Article  Google Scholar 

  • Takahama U (1988) Oxidation of flavonoids by hydrogen peroxide in epidermal guard cells of Vicia faba L. Plant Cell Physiol 29:433–438

    CAS  Google Scholar 

  • Takahama U, Oniki T (1997) A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. Physiol Plant 101:845–852

    Article  CAS  Google Scholar 

  • Takeuchi Y, Kubo H, Kasahara H, Sakaki T (1996) Adaptive alterations in the activities of scavengers of active oxygen in cucumber cotyledons irritated with UV-B. J Plant Physiol 147:589–592

    Article  CAS  Google Scholar 

  • Tegelberg R, Julkunen-Tiitto R, Aphalo PJ (2001) The effects of long-term elevated UV-B on the growth and phenolics of field-grown silver birch (Betula pendula). Glob Chang Biol 7:839–848

    Article  Google Scholar 

  • Tegelberg R, Veteli T, Aphalo PJ, Julkunen-Tiitto R (2003) Clonal differences in growth and phenolics of willows exposed to elevated ultraviolet-B radiation. Basic Appl Ecol 4:219–228

    Article  CAS  Google Scholar 

  • Tscharntke T, Thiessen S, Dolch R, Boland W (2001) Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa. Biochem Syst Ecol 29:1025–1047

    Article  CAS  Google Scholar 

  • Vaarama A, Valanne T (1973) On the taxonomy, biology and origin of Betula tortuosa Ledeb. Rep Kevo Sub Res Stn 10:70–84

    Google Scholar 

  • van Ooik T, Rantala MJ, Saloniemi I (2007) Diet-mediated effects of heavy metal pollution on growth and immune response in the geometrid moth, Epirrita autumnata. Environ Poll 145:348–354

    Article  Google Scholar 

  • van Ooik T, Pausio S, Rantala MJ (2008) Direct effects of heavy metal pollution on the immune function of a geometrid moth. Chemosphere 71:1840–1844

    Article  PubMed  Google Scholar 

  • Veteli TO, Tegelberg R, Pusenius J, Sipura M, Julkunen-Tiitto R, Aphalo PJ, Tahvanainen J (2003) Interactions between willows and insect herbivores under enhanced ultraviolet-B radiation. Oecologia 137:312–320

    Article  CAS  PubMed  Google Scholar 

  • Wilson KE, Wilson MI, Greenberg BM (1998) Identification of the flavonoid glycosides that accumulate in response to ultraviolet-B radiation. Photochem Photobiol 67:547–553

    Article  CAS  Google Scholar 

  • Wu G, Shortt BJ, Lawrence EB, Elaine E, Fitzsimmons K, Shah D (1995) Disease resistance conferred by expression of a gene encoding H2O2-generating glucose oxidase in transgenic potato plants. Plant Cell 7:1357–1368

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang S, Ruuhola T, Haviola S, Rantala MJ (2007a) Temperature as a modifier of plant–herbivore interaction. J Chem Ecol 33:463–475

    Article  CAS  PubMed  Google Scholar 

  • Yang S, Ruuhola T, Rantala MJ (2007b) Impacts of starvation on immune defence and other life history traits of an outbreaking geometrid, Epirrita autumnata: a possible ultimate trigger of the crash phase of population cycle. Ann Zool Fenn 44:89–96

    Google Scholar 

Download references

Acknowledgments

We thank Hanni Sikanen and other members of the staff of Punkaharju Research Station (the Finnish Forest Research Institute Metla) for help and assistance in the research work. We also want to express our warmest gratitude to Jaakko Heinonen for guidance in statistical analyses. Jo Short kindly checked the English of the manuscript. This study was financially supported by the Academy of Finland and the foundation of Kone and Väinö Tanner, Suomen Kulttuurirahasto, Suomen Perhostutkijainseura ry and Suomen Biologian Seura Vanamo ry. The authors declare that they have no conflict of interest. Our experiments comply with the current laws of Finland.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Teija Ruuhola.

Additional information

Communicated by Evan DeLucia.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anttila, U., Julkunen-Tiitto, R., Rousi, M. et al. Effects of elevated ultraviolet-B radiation on a plant–herbivore interaction. Oecologia 164, 163–175 (2010). https://doi.org/10.1007/s00442-010-1658-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1658-5

Keywords

Navigation