Oecologia

, Volume 138, Issue 4, pp 505–512 | Cite as

Solar UV-B radiation affects leaf quality and insect herbivory in the southern beech tree Nothofagus antarctica

  • M. Cecilia Rousseaux
  • Riitta Julkunen-Tiitto
  • Peter S. Searles
  • Ana L. Scopel
  • Pedro J. Aphalo
  • Carlos L. Ballaré
Ecophysiology

Abstract

We examined the effects of solar ultraviolet-B (UV-B) radiation on plant-insect interactions in Tierra del Fuego (55°S), Argentina, an area strongly affected by ozone depletion because of its proximity to Antarctica. Solar UV-B under Nothofagus antarctica branches was manipulated using a polyester plastic film to attenuate UV-B (uvb−) and an Aclar film to provide near-ambient UV-B (uvb+). The plastic films were placed on both north-facing (i.e., high solar radiation in the Southern Hemisphere) and south-facing branches. Insects consumed 40% less leaf area from north- than from south-facing branches, and at least 30% less area from uvb+ branches than from uvb− branches. The reduced herbivory on leaves from uvb+ branches occurred for both branch orientations. Leaf mass per area increased and relative water content decreased on north- versus south-facing branches, while no differences were apparent between the UV-B treatments. Solar UV-B did lead to lower gallic acid concentration and higher flavonoid aglycone concentration in uvb+ leaves relative to uvb− leaves. Both the flavonoid aglycone and quercetin-3-arabinopyranoside were higher on north-facing branches. In laboratory preference experiments, larvae of the dominant insect in the natural community, Geometridae “Brown” (Lepidoptera), consumed less area from field-grown uvb+ leaves than from uvb− leaves in 1996–97, but not in 1997–98. Correlation analyses suggested that the reduction in insect herbivory in the field under solar UV-B may be mediated in part by the UV-B effects on gallic acid and flavonoid aglycone.

Keywords

Flavonoids Gallic acid Herbivory  Nothofagus Ozone depletion 

References

  1. Ballaré CL, Scopel AL, Stapleton AE, Yanovsky MJ (1996) Solar ultraviolet-B radiation affects seedling emergence, DNA integrity, plant morphology, growth rate, and attractiveness to herbivore insects in Datura ferox. Plant Physiol 112:161–170PubMedGoogle Scholar
  2. Ballaré CL, Rousseaux MC, Searles PS, Zaller JG, Giordano CV, Robson TM, Caldwell MM, Sala OE, Scopel AL (2001) Impacts of solar ultraviolet-B radiation on terrestrial ecosystems of Tierra del Fuego (southern Argentina) An overview of recent progress. J Photochem Photobiol B Biol 62:67–77CrossRefGoogle Scholar
  3. Beggs CJ, Wellmann E (1985) Analysis of light-controlled anthocyanin formation in coleoptiles of Zea mays L.: the role of UV-B, blue, red, and far-red light. Photochem Photobiol 41:481–486Google Scholar
  4. Björkman O (1981) Responses to different quantum flux densities. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of plant physiology (NS, vol 12 A). Springer, Berlin Heidelberg New York, pp 57–107Google Scholar
  5. Bothwell ML, Sherbot DMJ, Pollock CM (1994) Ecosystem response to solar ultraviolet-B radiation: influence of trophic-level interactions. Science 265:97–100Google Scholar
  6. Buck N, Callaghan TV (1999) The direct and indirect effects of enhanced UV-B on the moth caterpillar Epirrita autumnata. Ecol Bull 47:68–76Google Scholar
  7. Caldwell MM, Searles PS, Flint SD, Barnes PW (1999) Terrestrial ecosystem responses to solar UV-B radiation mediated by vegetation, microbes and abiotic photochemistry. In: Press MC, Scholes JD, Barker MG (eds) Physiological plant ecology. Blackwell Science, Oxford, pp 241–262Google Scholar
  8. 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 climate change factors. Photochem Photobiol Sci 2:29–38CrossRefPubMedGoogle Scholar
  9. Choong MF (1996) What makes a leaf tough and how this affects the pattern of Castanopsis fissa leaf consumption by caterpillars. Funct Ecol 10:668–674Google Scholar
  10. De la Rosa TM, Julkunen-Tiitto R, Lehto T, Aphalo PJ (2001) Secondary metabolites and nutrient concentrations in silver birch seedlings under five levels of daily UV-B exposure and two relative nutrient addition rates. New Phytol 150:121–131CrossRefGoogle Scholar
  11. Dudt JF, Shure DJ (1994) The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology 75:86–98Google Scholar
  12. FAO (1985) Plant production and protection (Series N24). Food and Agricultural Organization, RomeGoogle Scholar
  13. Frederick JE, Díaz SB, Smolskaia I, Esposito W, Lucas T, Booth C (1994) Ultraviolet solar radiation in the high latitudes of South America. Photochem Photobiol 60:356–362Google Scholar
  14. Gwynn-Jones D, Lee JA, Callaghan TV (1997) Effects of enhanced UV-B radiation and elevated carbon dioxide concentrations on a sub-arctic forest heath ecosystem. Plant Ecol 128:242–249CrossRefGoogle Scholar
  15. Hanley ME, Lamont BB (2002) Relationships between physical and chemical attributes of congeneric seedlings: how important is seedling defence? Funct Ecol 16:216–222CrossRefGoogle Scholar
  16. Harborne JB (1988) The flavonoids. Advances in research since 1980. Chapman and Hall, New YorkGoogle Scholar
  17. Hedin PA, Waage SK (1986) Roles of flavonoids in plant resistance to insects. In: Cody V, Middleton E Jr, Harborne JB (eds) Plant flavonoids in biology and medicine: biochemical, pharmacological, and structure-activity relationships. Liss, New York, pp 87–100Google Scholar
  18. Izaguirre MM, Scopel AL, Baldwin IT, Ballaré CL (2003) Convergent responses to stress, solar ultraviolet-B radiation and Manduca sexta herbivory elicit overlapping transcriptional responses in field-grown plants of Nicotiana longiflora. Plant Physiol 132:1755–1767CrossRefPubMedGoogle Scholar
  19. Julkunen-Tiitto R, Rousi M, Bryant J, Sorsa S, Keinaenen M, Sikanen H (1996) Chemical diversity of several Betulaceae species: Comparison of phenolics and terpenoids in northern birch stems. Trees 11:16–22CrossRefGoogle Scholar
  20. Kause A, Ossipov V, Haukioja E, Lempa K, Hanhimaki S, Ossipova S (1999) Multiplicity of biochemical factors determining quality of growing birch leaves. Oecologia 120:102–112CrossRefGoogle Scholar
  21. 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 26:1–12CrossRefGoogle Scholar
  22. Lempa K, Martel J, Koricheva J, Haukioja E, Ossipov V, Ossipova S, Pihlaja K (2000) Covariation of fluctuating asymmetry, herbivory and chemistry during birch leaf expansion. Oecologia 122:354–360CrossRefGoogle Scholar
  23. 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 120:20–28Google Scholar
  24. Louda SM, Dixon PM, Huntly N (1987) Herbivory in sun versus shade at a natural meadow-woodland ecotone in the Rocky Mountains. Vegetatio 72:141–149Google Scholar
  25. 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 96:980–985CrossRefPubMedGoogle Scholar
  26. Mazza CA, Izaguirre MM, Zavala J, Scopel AL, Ballaré CL (2002) Insect perception of ambient ultraviolet-B radiation. Ecol Lett 5:722–726CrossRefGoogle Scholar
  27. McCloud ES, Berenbaum MR (1994) Stratospheric ozone depletion and plant-insect interactions: effects of UVB radiation on foliage quality of Citrus jambhiri for Trichoplusia ni. J Chem Ecol 20:525–539Google Scholar
  28. McCloud ES, Berenbaum MR (1999) Effects of enhanced UV-B radiation on a weedy forb ( Plantago lanceolata) and its interactions with a generalist and specialist herbivore. Entomol Exp Appl 93:233–247CrossRefGoogle Scholar
  29. McQuillan PB (1993) Nothofagus (Fagaceae) and its invertebrate fauna: an overview and preliminary synthesis. Biol J Linn Soc 49:317–354CrossRefGoogle Scholar
  30. Mole S, Waterman P (1988) Light-induced variation in phenolic levels in foliage of rain-forest plants. II. Potential significance to herbivores. J Chem Ecol 14:23–34Google Scholar
  31. Moore D (1983) Flora of Tierra del Fuego. Missouri Botanical Garden, St. LouisGoogle Scholar
  32. Rousseaux MC, Ballaré CL, Scopel AL, Searles PS, Caldwell MM (1998) Solar ultraviolet-B radiation affects plant-insect interactions in a natural ecosystem of Tierra del Fuego (southern Argentina). Oecologia 116:528–535CrossRefGoogle Scholar
  33. Rousseaux MC, Ballaré CL, Giordano CV, Scopel AL, Zima AM, Szwarcberg-Bracchitta M, Searles PS, Caldwell MM, Díaz SB (1999) Ozone depletion and UVB radiation: impact on plant DNA damage in southern South America. Proc Natl Acad Sci USA 96:15310–15315CrossRefPubMedGoogle Scholar
  34. Rousseaux MC, Scopel AL, Searles PS, Caldwell MM, Sala OE, Ballaré CL (2001) Responses to solar ultraviolet-B radiation in a shrub-dominated natural ecosystem of Tierra del Fuego (southern Argentina). Global Change Biol 7:467–478CrossRefGoogle Scholar
  35. Searles PS, Flint SD, Caldwell MM (2001) A meta-analysis of plant field studies simulating stratospheric ozone depletion. Oecologia 127:1–10CrossRefGoogle Scholar
  36. Searles PS, Flint SD, Díaz SB, Rousseaux MC, Ballaré CL, Caldwell MM (2002) Plant response to solar ultraviolet-B radiation in a southern South American Sphagnum peatland. J Ecol 90:704–713CrossRefGoogle Scholar
  37. Spagarino C, Pastur GM, Peri PL (2001) Changes in Nothofagus pumilio forest biodiversity during the forest management cycle. 1. Insects. Biodivers Conserv 10:2077–2092CrossRefGoogle Scholar
  38. Tegelberg R, Julkunen-Tiitto R (2001) Quantitative changes in secondary metabolites of dark-leaved willow ( Salix myrsinifolia) exposed to enhanced ultraviolet-B radiation. Physiol Plant 113:541–547CrossRefGoogle Scholar
  39. Warren JM, Bassman JH, Eigenbrode S (2002) Leaf chemical changes induced in Populus trichocarpa by enhanced UV-B radiation and concomitant effects on herbivory by Chrysomela scripta (Coleoptera: Chrysomelidae). Tree Physiol 22:1137–1146PubMedGoogle Scholar
  40. Zavala JA, Scopel AL, Ballaré CL (2001) Effects of ambient UV-B radiation on soybean crops: Impact on leaf herbivory by Anticarsi gemmatalis. Plant Ecol 156:1–10CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • M. Cecilia Rousseaux
    • 1
    • 5
  • Riitta Julkunen-Tiitto
    • 2
  • Peter S. Searles
    • 3
    • 6
  • Ana L. Scopel
    • 1
  • Pedro J. Aphalo
    • 4
  • Carlos L. Ballaré
    • 1
  1. 1.IFEVAConsejo Nacional de Investigaciones Científicas y Técnicas and Universidad de Buenos AiresBuenos AiresArgentina
  2. 2.Department of BiologyUniversity of JoensuuJoensuuFinland
  3. 3.Department of Rangeland Resources and The Ecology CenterUtah State UniversityUSA
  4. 4.Department of Biological and Environmental ScienceUniversity of JyväskyläJyväskyläFinland
  5. 5.CRILARConsejo Nacional de Investigaciones Científicas y TécnicasLa RiojaArgentina
  6. 6.CRILARConsejo Nacional de Investigaciones Científicas y TécnicasLa RiojaArgentina

Personalised recommendations