Abstract
The exposure of plants to abiotic stresses like air pollutants may increase their susceptibility to herbivores. However, abiotic stresses often induce the accumulation of phenolic compounds that may have adverse effects on plant-eating animals. In this study, we examined the effects of long-term (14 years) deposition of simulated acid rain (H2SO4) and heavy metals (CuNi) on the plant–herbivore interaction. The used species were well-known model species of plant–herbivore interaction, namely the mountain birch (Betula pubescens ssp. czerepanovii) and autumnal moth (Epirrita autumnata). The study set-up was factorial with four combinations of two treatments: −acid−CuNi, +acid−CuNi, −acid+CuNi, and +acid+CuNi. The deposition of pollutants had no marked effects on the growth, survival, or immune function of the autumnal moth although the chemistry of birch leaves was markedly affected. The concentrations of gallic acid, chlorogenic acid, three of hydrolyzable tannins (HTs), and quercetin glycosides were induced by the acid rain treatment when compared to leaves not treated with acid rain. We concluded that an increase in compounds with high redox capacity was a defense against oxidative stress caused by pollution treatments. We suggested that pollution might have increased the deposition of non-phenolic antioxidants like ascorbate that diminish the adverse effects of phenolics on herbivores. We also stated that abiotic stresses might play an equally strong role in the evolution of phenolics than herbivory if not larger.
Similar content being viewed by others
References
Abramoff MD, Magelhaes JD (2004) Image processing with ImageJ. Biophot Int 11:36–42
Alstad DN, Edmunds GF (1982) Effects of air-pollutants on insect populations. Annu Rev Ent 27:369–384
Anttila U, Julkunen-Tiitto R, Rousi M, Yang SY, Rantala MJ, Ruuhola T (2010) Effects of elevated ultraviolet-B radiation on a plant–herbivore interaction. Oecologia 164:163–175
Badejo AA, Fujikawa Y, Esaka M (2009) Gene expression of ascorbic acid biosynthesis related enzymes of the Smirnoff–Wheeler pathway in acerola (Malpighia glabra). J Plant Physiol 166:652–660
Barbehenn RV, Burmgarner SL, Martin MM (2001) Antioxidant defenses in caterpillars: role of the ascorbate-recycling system in the midgut lumen. J Insect Physiol 47:349–357
Barbehenn R, Cheek S, Gasperut A, Lister E, Maben R (2005) Phenolic compounds in red oak and sugar maple leaves have prooxidant activities in the midgut fluids of Malacosoma disstria and Orgyia leucostigma caterpillars. J Chem Ecol 31:969–988
Barbehenn RV, Jones CP, Hagerman AE, Karonen M, Salminen JP (2006a) Ellagitannins have greater oxidative activities than condensed tannins and galloyl glucoses at high pH: potential impact on caterpillars. J Chem Ecol 32:2253–2267
Barbehenn RV, Jones CP, Karonen M, Salminen JP (2006b) Tannin composition affects the oxidative activities of tree leaves. J Chem Ecol 32:2235–2251
Barbehenn R, Weir Q, Salminen JP (2008) Oxidation of ingested phenolics in the tree-feeding caterpillar Orgyia leucostigma depends on foliar chemical composition. J Chem Ecol 34:748–756
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
Bi JL, Felton GW, Murphy JB, Howles PA, Dixon RA, Lamb CJ (1997) Do plant phenolics confer resistance to specialist and generalist insect herbivores? J Agric Food Chem 45:4500–4504
Bittner S (2006) When quinones meet amino acids: chemical, physical and biological consequences. Amino Acids 30:205–224
Carmona D, Lajeunesse MJ, Johnson MTJ (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367
Chacón P, Armesto JJ (2006) Do carbon-based defenses reduce foliar damage? Habitat-related effects on tree seedling performance in a temperate rainforest of Chiloé Island, Chile. Oecologia 146:555–565
Close DC, McArthur C (2002) Rethinking the role of many plant phenolics—protection from photodamage not herbivores? Oikos 99:166–172
Conklin PI, Barth C (2004) Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. Plant Cell Environ 27:959–970
Diaz J, Bernal A, Pomar F, Merino F (2001) Induction of shikimate dehydrogenase and peroxidase in pepper (Capsicum annuum L.) seedlings in response to copper stress and its relation to lignification. Plant Sci 161:179–188
Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608
Felton GW, Donato KK, 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
Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643
Grassmann J, Hippeli S, Elstner EF (2002) Plant’s defense and its benefits for animals and medicine: role of phenolics and terpenoids in avoiding oxygen stress. Plant Physiol Biochem 40:471–478
Hanhimäki S, Senn J, Haukioja E (1994) Performance of insect herbivores on hybridizing trees—the case of the sub-arctic birches. J Anim Ecol 63:163–175
Haukioja E (1980) On the role of plant defenses in the fluctuation of herbivore populations. Oikos 35:202–213
Haukioja E (1991) Induction of defenses in trees. Annu Rev Entomol 36:25–42
Heim KE, Tagliaferro AR, Bobilya DJ (2002) Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J Nutr Biochem 13:572–584
Izquierdo AM, Torres MPN, Jimenez GS, Sosa FC (2011) Changes in biomass allocation and phenolic compounds accumulation due to the effect of light and nitrate supply in Cecropia peltata plants. Acta Physiol Plant 33:2135–2147
Jiravanichpaisal P, Lee BL, Söderhäll K (2006) Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211:213–236
Johnson KS, Felton GW (2001) Plant phenolics as dietary antioxidants for herbivorous insects: a test with genetically modified tobacco. J Chem Ecol 27:2579–2597
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 Pollut 137:404–414
Kapari L, Haukioja E, Rantala MJ, Ruuhola T (2006) Defoliating insect immune defense interacts with induced plant defense during a population outbreak. Ecology 87:291–296
Karban R (2011) The ecology and evolution of induced resistance against herbivores. Funct Ecol 25:339–347
Klemola N, Klemola T, Rantala MJ, Ruuhola T (2007) Natural host–plant quality affects immune defense of an insect herbivore. Entomol Exp Appl 123:167–176
Kondo N, Kawashima M (2000) Enhancement of the tolerance to oxidative stress in cucumber (Cucumis sativus L.) seedlings by UV-B irradiation: possible involvement of phenolic compounds and antioxidative enzymes. J Plant Res 113:311–317
Koricheva J, Haukioja E (1995) Variations in chemical-composition of birch foliage under air- pollution stress and their consequences for Eriocrania miners. Environ Pollut 88:41–50
Koricheva J, Roy S, Vranjic JA, Haukioja E, Hughes PR, Hänninen O (1997) Antioxidant responses to simulated acid rain and heavy metal deposition in birch seedlings. Environ Pollut 95:249–258
Koricheva J, Larsson S, Haukioja E (1998) Insect performance on experimentally stressed woody plants: a meta-analysis. Annu Rev Ent 43:195–216
Kováčik J, Klejdus B, Backor M (2009) Phenolic metabolism of Matricaria chamomilla plants exposed to nickel. J Plant Physiol 166:1460–1464
Kraaijeveld AR, Godfray HCJ (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278–280
Kranthi S, Kranthi KR, Wanjari RR (2003) Influence of semilooper damage on cotton host-plant resistance to Helicoverpa armigera (Hub). Plant Sci 164:157–163
Labieniec M, Gabryelak T, Falcioni G (2003) Antioxidant and pro-oxidant effects of tannins in digestive cells of the freshwater mussel Unio tumidus. Mutat Res Gen Tox En 539:19–28
Lavid N, Schwartz A, Lewinsohn E, Tel-Or E (2001) Phenols and phenol oxidases are involved in cadmium accumulation in the water plants Nymphoides peltata (Menyanthaceae) and Nymphaeae (Nymphaeaceae). Planta 214:189–195
Markham KR, Tanner GJ, Caasi-Lit, M, Whitecross MI, Nayudu M, Mitchhell KA (1998) Possible protective role of 3′4′ -dihydroxyflavones induced by enhanced UV-B in a UV-tolerant rice cultivar. Phytochemistry 49:1913–1919
Mcleod AR, Holland MR, Shaw PJA, Sutherland PM, Darrall NM, Skeffington RA (1990) Enhancement of nitrogen deposition to forest trees exposed to SO2. Nature 347:277–279
Metlen KL, Aschehoug ET, Callaway RM (2009) Plant behavioural ecology: dynamic plasticity in secondary metabolites. Plant Cell Environ 32:641–653
Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15:523–530
Moilanen J, Salminen JP (2008) Ecologically neglected tannins and their biologically relevant activity: chemical structures of plant ellagitannins reveal their in vitro oxidative activity at high pH. Chemoecology 18:73–83
Munoz-Munoz JL, Garcia-Molina F, Garcia-Ruiz PA, Arribas E, Tudela J, Garcia-Canovas F, Rodriguez-Lopez JN (2009) Enzymatic and chemical oxidation of trihydroxylated phenols. Food Chem 113:435–444
Neuvonen S, Lindgren M (1987) The effect of simulated acid rain on performance of the aphid Euceraphis betulae (Koch) on silver birch. Oecologia 74:77–80
Neuvonen S, Saikkonen K, Haukioja E (1990) Simulated acid rain reduces the susceptibility of the European pine sawfly (Neodiprion sertifer) to its nuclear polyhedrosis virus. Oecologia 83:209–212
Ossipov V, Klemola T, Ruohomäki K, Salminen JP (2010) Hydrolysable tannins as a factor of rapid inducible resistance of mountain birch trees to herbivorous insects. Polyphe Commun 1:307–308
Palokangas P, Neuvonen S, Haapala S (1995) Effects of simulated acid rain on growth and susceptibility to predation of Phratora polaris (Col, Chrysomelidae). Environ Pollut 89:67–71
Peltonen P (2007) Impact of elevated O3 and CO2 concentrations on phenolic compounds of birch (Betula pendula Roth): implications for herbivorous insects and detritivorous soil animals. University of Joensuu, PhD dissertations in Biology, Joensuu
Peltonen P, Vapaavuori E, Julkunen-Titto R (2005) Accumulation of phenolic compounds in birch leaves is changed by elevated carbon dioxide and ozone. Glob Change Biol 11:1305–1324
Peltonen P, Julkunen-Tiitto R, Vapaavuori E, Heinonen J, Holopainen J (2010) Do elevated atmospheric CO2 and O3 affect food quality and performance of folivorous insects on silver birch? Glob Change Biol 16:918–935
Pennanen T, Perkiomäki J, Kiikkila O, Vanhala P, Neuvonen S, Fritze H (1998) Prolonged, simulated acid rain and heavy metal deposition: separated and combined effects on forest soil microbial community structure. FEMS Microbiol Ecol 27:291–300
Pukacka S, Pukacki PM (2000) Seasonal changes in antioxidant level of Scots pine (Pinus sylvestris L.) needles exposed to industrial pollution. I. Ascorbate and thiol content. Acta Physiol Plant 22:451–456
Rantala MJ, Roff DA (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean field cricket, Gryllus bimaculatus. Funct Ecol 19:323–330
Rantala MJ, Roff DA (2007) Inbreeding and extreme outbreeding causes sex differences in immune defense and life history traits in Epirrita autumnata. Heredity 98:329–336
Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J (2002) Do pheromones reveal male immunocompetence? Proc R Soc Lond B 269:1681–1685
Reinert RA (1984) Plant-response to air pollutant mixtures. Annu Rev Phytopathol 22:421–442
Rennenberg H, Gessler A (2001) Acid rain. Nature encyclopedia of life sciences. Nature Publishing Group, London
Ruohomäki K, Kaitaniemi P, Kozlov MV, Tammaru T, Haukioja E (1996) Density and performance of Epirrita autumnata (Lepidoptera: Geometridae) along three air pollution gradients in northern Europe. J Appl Ecol 33:773–785
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
Ruuhola T, Yang S (2006) Wound-induced oxidative responses in mountain birch leaves. Ann Bot 97:29–37
Ruuhola T, Salminen JP, Haviola S, Yang S, Rantala MJ (2007) Immunological memory of mountain birches: the effects of phenolics on the performance of the autumnal moth depend on the herbivory history of trees. J Chem Ecol 33:1160–1176
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
Ruuhola T, Rantala LM, Neuvonen S, Yang S, Rantala MJ (2009) Effects of long-term simulated acid rain on a plant-herbivore interaction. Basic Appl Ecol 10:589–596
Ruuhola T, Yang S, Rantala MJ (2010) Increase in the substrate availability decreases phenoloxidase activity in the autumnal moth, Epirrita autumnata. Chemoecology 20:11–18
Ryan KG, Markham KR, Bloor SJ, Bradley JM, Mitchell KA, Jordan BR (1998) UVB radiation induced increase in quercetin:kaempferol ratio in normal and transgenic lines of Petunia. Photoch. Photobiol 68:323–330
Salminen JP, Ossipov V, Loponen J, Haukioja E, Pihlaja K (1999) Characterisation of hydrolysable tannins from leaves of Betula pubescens by high-performance liquid chromatography–mass spectrometry. J Chromatogr A 864:283–291
Salminen JP, Ossipov V, Haukioja E, Pihlaja K (2001) Seasonal variation in the content of hydrolysable tannins in leaves of Betula pubescens. Phytochemistry 57:15–22
Salminen JP, Ossipov V, Pihlaja K (2002) Distribution of hydrolysable tannins in the foliage of Finnish birch species. Z Naturforsch C 57:248–256
Seyyednejad SM, Koochak H (2010) A survey on biochemical effects of industrial air pollution on Eucalyptus camaldulensis Dehnh. J Food Agr Environ 8:1272–1275
Sgherri C, Cosi E, Navari-Izzo F (2003) Phenols and antioxidative status of Raphanus sativus grown in copper excess. Physiol Plant 118:21–28
Shahidi F, Chandrasekara A (2010) Hydroxycinnamates and their in vitro and in vivo antioxidant activities. Phytochem Rev 9:147–170
Sipura M, Tahvanainen J (2000) Shading enhances the quality of willow leaves to leaf beetles—but does it matter? Oikos 91:550–558
Söderhäll K, Cerenius L (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 10:23–28
Suomela J, Neuvonen S (1997) Effects of long-term simulated acid rain on suitability of mountain birch for Epirrita autumnata (Geometridae). Can J For Res 27:248–256
Takahama U, Oniki T (1997) A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. Physiol Plant 101:845–852
Tamas L, Huttova J, Mistrik I, Simonovicova M, Siroka B (2006) Aluminium-induced drought and oxidative stress in barley roots. J Plant Physiol 163:781–784
Tuovinen JP, Laurila T, Lattila H, Ryaboshapko A, Brukhanov P, Korolev S (1993) Impact of the sulfur dioxide sources in the Kola-Peninsula on air-quality in northernmost Europe. Atmos Environ A Gen Top 27:1379–1395
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 Pollut 145:348–354
van Ooik T, Pausio S, Rantala MJ (2008) Direct effects of heavy metal pollution on the immune function of a geometrid moth, Epirrita autumnata. Chemosphere 71:1840–1844
Wang JJ, Zhao ZM, Zhang JP (2004) The host plant-mediated impact of simulated acid rain on the development and reproduction of Tetranychus cinnabarinus (Acari, Tetranychidae). J Appl Entomol 128:397–402
Washburn JO, Kirkpatrick BA, Volkman LE (1996) Insect protection against viruses. Nature 383:767
White TCR (1974) Hypothesis to explain outbreaks of looper caterpillars, with special reference to populations of Selidosema suavis in a plantation of Pinus radiata in New-Zealand. Oecologia 16:279–301
White TCR (1984) The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63:90–105
Yang S, Ruuhola T, Rantala MJ (2007) Impact of starvation on immune defense and other life-history traits of an outbreaking geometrid, Epirrita autumnata: a possible causal trigger for the crash phase of population cycle. Ann Zool Fenn 44:89–96
Yang S, Ruuhola T, Haviola S, Rantala MJ (2008) Effects of host plant shift on immune and other key life history traits of an eruptive Geometrid, Epirrita autumnata (Borkhausen). Ecol Entomol 33:510–516
Zancani M, Nagy G (2000) Phenol-dependent H2O2 breakdown by soybean root plasma membrane-bound peroxidase is regulated by ascorbate and thiols. J Plant Physiol 15:259–299
Zobel A, Nigthswander JE (1991) Accumulation of phenolic compounds in the necrotic areas of Austrian and red pine needles after spraying with sulphuric acid: a possible bioindicator of air pollution. New Phytol 117:565–574
Acknowledgments
We thank the staff of the Kevo Subarctic Research Institute for help and providing pleasant working facilities and all those who have contributed to the long-term simulated acid rain and heavy metal pollution experiment. We thank Sanna Haviola for assistance in the fieldwork and Line Nybakken for invaluable comments concerning the MS. This research was made possible by finance granted by the Academy of Finland to TR and MJR and by the Kone Foundation. William Sillitoe kindly checked the English of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
van Ooik, T., Rantala, M.J., Salminen, JP. et al. The effects of simulated acid rain and heavy metal pollution on the mountain birch–autumnal moth interaction. Chemoecology 22, 251–262 (2012). https://doi.org/10.1007/s00049-012-0114-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00049-012-0114-x