Skip to main content
SpringerLink
Log in

Phenolic Compounds in Red Oak and Sugar Maple Leaves Have Prooxidant Activities in the Midgut Fluids of Malacosoma disstria and Orgyia leucostigma Caterpillars

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

Abstract

Phenolic compounds are generally believed to be key components of the oxidative defenses of plants against pathogens and herbivores. However, phenolic oxidation in the gut fluids of insect herbivores has rarely been demonstrated, and some phenolics could act as antioxidants rather than prooxidants. We compared the overall activities of the phenolic compounds in red oak (Quercus rubra) and sugar maple (Acer saccharum) leaves in the midgut fluids of two caterpillar species, Malacosoma disstria (phenolic-sensitive) and Orgyia leucostigma (phenolic-tolerant). Three hypotheses were examined: (1) ingested sugar maple leaves produce higher levels of semiquinone radicals (from phenolic oxidation) in caterpillar midgut fluids than do red oak leaves; (2) O. leucostigma maintains lower levels of phenolic oxidation in its midgut fluids than does M. disstria; and (3) phenolic compounds in tree leaves have overall prooxidant activities in the midgut fluids of caterpillars. Sugar maple leaves had significantly lower ascorbate:phenolic ratios than did red oak leaves, suggesting that phenolics in maple would oxidize more readily than those in oak. As expected, semiquinone radicals were at higher steady-state levels in the midgut fluids of both caterpillar species when they fed on sugar maple than on red oak, consistent with the first hypothesis. Higher semiquinone radical levels were also found in M. disstria than in O. leucostigma, consistent with the second hypothesis. Finally, semiquinone radical formation was positively associated with two markers of oxidation (protein carbonyls and total peroxides). These results suggest that the complex mixtures of phenolics in red oak and sugar maple leaves have overall prooxidant activities in the midgut fluids of M. disstria and O. leucostigma caterpillars. We conclude that the oxidative defenses of trees vary substantially between species, with those in sugar maple leaves being especially active, even in phenolic-tolerant herbivore species.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • S. Ahmad (1992) ArticleTitleBiochemical defence of pro-oxidant plant allelochemicals by herbivorous insects Biochem. Syst. Ecol. 20 269–296

    Google Scholar 

  • H. M. Appel (1993) ArticleTitlePhenolics in ecological interactions: The importance of oxidation J. Chem. Ecol. 19 1521–1552

    Google Scholar 

  • H. M. Appel J. C. >Schultz (1994) ArticleTitleOak tannins reduce effectiveness of Thuricide (Bacillus thuringiensis) in gypsy moth (Lepidoptera: Lymantriidae) J. Econ. Entomol. 87 1736–1742

    Google Scholar 

  • Baker, W. L. 1972. Eastern Forest Insects. USDA Miscellaneous Publication no. 1175, Washington, DC..

  • R. V. Barbehenn (2003) ArticleTitleAntioxidants in grasshoppers: Higher levels defend the midgut tissues of a polyphagous species than a graminivorous species J. Chem. Ecol. 29 683–702

    Google Scholar 

  • R. V. Barbehenn M. M. Martin (1992) ArticleTitleThe protective role of the peritrophic membrane in the tannin-tolerant larvae of Orgyia leucostigma (Lepidoptera) J. Insect Physiol. 38 973–980

    Google Scholar 

  • R. V. Barbehenn M. M. Martin (1994) ArticleTitleTannin sensitivity in Malacosoma disstria: Roles of the peritrophic envelope and midgut oxidation J. Chem. Ecol. 20 1985–2001

    Google Scholar 

  • R. V. Barbehenn M. M. Martin A. E. Hagerman (1996) ArticleTitleReassessment of the roles of the peritrophic envelope and hydrolysis in protecting polyphagous grasshoppers from ingested hydrolyzable tannins J. Chem. Ecol. 22 1911–1929

    Google Scholar 

  • R. V. Barbehenn S. L. Bumgarner E. F. Roosen M. M. Martin (2001) ArticleTitleAntioxidant defenses in caterpillars: Role of the ascorbate-recycling system in the midgut lumen J. Insect Physiol. 47 349–357

    Google Scholar 

  • R. V. Barbehenn A. C. Walker F. Uddin (2003) ArticleTitleAntioxidants in the midgut fluids of a tannin-tolerant and a tannin-sensitive caterpillar: Effects of seasonal changes in tree leaves J. Chem. Ecol. 29 1099–1116

    Google Scholar 

  • R. V. Barbehenn U. Poopat B. Spencer (2003) ArticleTitleSemiquinone and ascorbyl radicals in the gut fluids of caterpillars measured with EPR spectrometry Insect Biochem. Mol. Biol. 33 125–130

    Google Scholar 

  • J. L. Bi G. W. Felton (1995) ArticleTitleFoliar oxidative stress and insect herbivory: Primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance J. Chem. Ecol. 21 1511–1530

    Google Scholar 

  • J. L. Bi J. B. Murphy G. W. Felton (1997) ArticleTitleAntinutritive and oxidative components as mechanisms of induced resistance in cotton to Helicoverpa zea J. Chem. Ecol. 23 97–117

    Google Scholar 

  • L. Bravo (1998) ArticleTitlePolyphenols: Chemistry, dietary sources, metabolism, and nutritional significance Nutr. Rev. 56 317–333

    Google Scholar 

  • G. Buettner (1993) ArticleTitleThe pecking order of free radicals and antioxidants: Lipid peroxidation, α-tocopherol, and ascorbate Arch. Biochem. Biophys. 300 535–543

    Google Scholar 

  • E. Cadenas (1995) Mechanisms of oxygen activation and reactive oxygen species detoxification S. Ahmad (Eds) Oxidative Stress and Antioxidant Defenses in Biology Chapman and Hall New York 1–61

    Google Scholar 

  • A. T. Canada E. Giannella T. D. Nguyen R. P. Mason (1990) ArticleTitleThe production of reactive oxygen species by dietary flavonols Free Radic. Biol. Med. 9 441–449

    Google Scholar 

  • S. S. Duffey M. J. Stout (1996) ArticleTitleAntinutritive and toxic components of plant defense against insects Arch. Insect Biochem. Physiol. 32 3–37

    Google Scholar 

  • G. W. Felton (1996) ArticleTitleNutritive quality of plant protein: Sources of variation and insect herbivore responses Arch. Insect Biochem. Physiol. 32 107–130

    Google Scholar 

  • G. W. Felton K. K. Donato R. J. Vecchio ParticleDel S. S. Duffey (1989) ArticleTitleActivation of plant polyphenol oxidases by insect feeding damage reduces the nutritive quality of foliage J. Chem. Ecol. 15 2667–2694

    Google Scholar 

  • G. W. Felton K. K. Donato R. M. Broadway S. S. Duffey (1992) ArticleTitleImpact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore J. Insect Physiol. 38 277–285

    Google Scholar 

  • G. Galati O. Sabzevari J. X. Wilson P. J. O’brien (2002) ArticleTitleProoxidant activity and cellular effects of the phenoxyl radicals of dietary flavonoids and other polyphenolics Toxicology 177 91–104

    Google Scholar 

  • T. W. Gant R. Ramakrishna R. P. Mason G. M. Cohen (1988) ArticleTitleRedox cycling and sulphydryl arylation; their relative importance in the mechanism of quinone cytotoxicity to isolated hepatocytes Chem.-Biol. Interact. 65 157–173

    Google Scholar 

  • H. D. Graham (1992) ArticleTitleStabilization of the Prussian blue color in the determination of polyphenols J. Agric. Food Chem. 40 801–805

    Google Scholar 

  • A. E. Hagerman K. M. Riedl G. A. Jones K. N. Sovik N. T. Ritchard P. W. Hartzfeld T. L. Riechel (1998) ArticleTitleHigh molecular weight plant polyphenolics (tannins) as biological antioxidants J. Agric. Food Chem. 46 188–189

    Google Scholar 

  • A. E. Hagerman R. T. Dean M. J. Davies (2003) ArticleTitleRadical chemistry of epigallocatechin gallate and its relevance to protein damage Arch. Biochem. Biophys. 414 115–120

    Google Scholar 

  • B. Halliwell J. M. C. Gutteridge (1999) Free Radicals in Biology and Medicine Oxford University Press Oxford

    Google Scholar 

  • J. B. Harborne (1985) Phenolics and plant defence C. F. Sumere ParticleVan P. J. Lea (Eds) The Biochemistry of Plant Phenolics Oxford University Press New York 393–408

    Google Scholar 

  • K. Hoover K. T. Kishida L. A. Digiorgio J. Workman S. A. Alaniz B. D. Hammock S. S. Duffey (1998) ArticleTitleInhibition of baculoviral disease by plant-mediated peroxidase activity and free radical generation J. Chem. Ecol. 24 1949–2001

    Google Scholar 

  • K. S. Johnson R. V. Barbehenn (1999) ArticleTitleOxygen levels in the gut lumens of herbivorous insects J. Insect Physiol. 46 897–903

    Google Scholar 

  • K. S. Johnson G. W. Felton (2001) ArticleTitlePlant phenolics as dietary antioxidants for herbivorous insects: A test with genetically modified tobacco J. Chem. Ecol. 27 2579–2597

    Google Scholar 

  • D. N. Karowe (1989) ArticleTitleDifferential effect of tannic acid on two tree-feeding Lepidoptera: Implications for theories of plant anti-herbivore chemistry Oecologia 80 507–512

    Google Scholar 

  • R. A. Larson (1995) Antioxidant mechanisms of secondary natural products S. Ahmad (Eds) Oxidant-Induced Stress and Antioxidant Defenses in Biology Chapman and Hall NewYork 210–237

    Google Scholar 

  • J. Lykkesfeldt S. Loft H. E. Poulsen (1995) ArticleTitleDetermination of ascorbic acid and dehydroascorbic acid in plasma by high-performance liquid chromatography with coulometric detection—Are they reliable biomarkers of oxidative stress? Anal. Biochem. 229 329–335

    Google Scholar 

  • D. Metadiewa A. K. Jaiswal N. Cenas E. Dickancaite N. Segura-Auilar (1999) ArticleTitleQuercetin may act as a cytotoxic prooxidant after its metabolic activation to semiquinone and quinoidal product Free Radic. Biol. Med. 26 107–116

    Google Scholar 

  • R. W. Nicol J. T. Arnason B. Helson M. M. Abou-Zaid (1997) ArticleTitleEffect of host and non-host trees on the growth and development of the forest tent caterpillar, Malacosoma disstria Hübner (Lepidoptera: Lasiocampidae) Can. Entomol. 129 995–1003

    Google Scholar 

  • J. Nourooz-Zadeh J. Tajaddini-Sarmadi S. P. Wolff (1994) ArticleTitleMeasurement of plasma hydroperoxide concentrations by the ferrous oxidation–xylenol orange assay in conjunction with triphenylphosphine Anal. Biochem. 220 403–409

    Google Scholar 

  • S. Ossipova V. Ossipov E. Haukioja J. Loponen K. Pihlaja (2001) ArticleTitleProanthocyanidins of mountain birch leaves: Quantification and properties Phytochem. Anal. 12 128–133

    Google Scholar 

  • R. S. Pardini (1995) ArticleTitleToxicity of oxygen from naturally occurring redox-active pro-oxidants Arch. Insect Biochem. Physiol. 29 101–118

    Google Scholar 

  • M. P. Price L. G. Butler (1977) ArticleTitleRapid visual estimation and spectrophotometric determination of tannin content of Sorghum grain J. Agric. Food Chem. 25 1268–1273

    Google Scholar 

  • G. J. Quinlan J. M. C. Gutteridge (2000) Carbonyl assay for oxidative damage to proteins N. Taniguchi J. M. C. Gutteridge (Eds) Experimental Protocols for Reactive Oxygen and Nitrogen Species Oxford University Press Oxford 257–258

    Google Scholar 

  • A. Z. Reznick L. Packer (1994) ArticleTitleOxidative damage to proteins: Spectrophotometric method for carbonyl assay Methods Enzymol. 233 357–371

    Google Scholar 

  • Y. Sakihama M. F. Cohen S. C. Grace H. Yamasaki (2002) ArticleTitlePlant phenolic antioxidant and prooxidant activities: Phenolics-induced oxidative damage mediated by metals in plants Toxicology 177 67–80

    Google Scholar 

  • J.-P. Salminen K. Lempa (2002) ArticleTitleEffects of hydrolyzable tannins on a herbivorous insect: Fate of individual tannins in insect digestive tract Chemocology 12 203–211

    Google Scholar 

  • J.-P. Salminen V. Ossipov J. Loponen E. Haukioja K. Pihlaja (1999) ArticleTitleCharacterization of hydrolyzable tannins from leaves of Betula pubescens by high-performance liquid chromatography–mass spectrometry J. Chromatrogr., A 864 283–291

    Google Scholar 

  • J.-P. Salminen T. Roslin M. Karonen J. Sinkkonen K. Pihlaja P. Pulkkinen (2004) ArticleTitleSeasonal variation in the content of hydrolysable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves J. Chem. Ecol. 30 1675–1693

    Google Scholar 

  • SAS Institute. 2000. The SAS System for Windows. Version 8e. SAS Institute, Cary, NC, USA

  • Stehr, W. F. and Cook, E. F. 1968. A revision of the genus Malacosoma Hübner in North America (Lepidoptera: Lasiocampidae): Systematics, biology, immatures, and parasites. Smithsonian Inst., U.S. Nat. Mus. Bull. no. 276

  • C. M. Stoscheck (1990) ArticleTitleIncreased uniformity in the response of the Coomassie blue G protein assay to different proteins Anal. Biochem. 184 111–116

    Google Scholar 

  • N. Sugihara T. Arakawa M. Ohnishi K. Furuno (1999) ArticleTitleAnti- and pro-oxidative effects of flavonoids on metal-induced lipid hydroperoxide-dependent lipid peroxidation in cultured hepatocytes loaded with α-linolenic acid Free Radic. Biol. Med. 27 1313–1323

    Google Scholar 

  • C. B. Summers G. W. Felton (1994) ArticleTitleProoxidant effects of phenolic acids on the generalist herbivore Helicoverpa zea (Lepidoptera: Noctuiidae): Potential mode of action for phenolic compounds in plant anti-herbivore chemistry Insect Biochem. Mol. Biol. 24 943–953

    Google Scholar 

  • R. L. Thiboldeaux R. L. Lindroth J. W. Tracy (1998) ArticleTitleEffects of juglone (5-hydroxy-1,4-naphthoquinone) on midgut morphology and glutathione status in Saturniid moth larvae Comp. Biochem. Physiol. 120 481–487

    Google Scholar 

  • R. H. Thompson (1964) Structure and reactivity of phenolic compounds J. B. Harborne (Eds) Biochemistry of Phenolic Compounds Academic Press New York 1–32

    Google Scholar 

  • J. A. Vinson J. Proch P. Bose (2001) ArticleTitleDetermination of quantity and quality of polyphenol antioxidants in foods and beverages Methods Enzymol. 335 103–114

    Google Scholar 

  • J. Wang C. P. Constabel (2004) ArticleTitlePolyphenol oxidase overexpression in transgenic Populus leaves enhances resistance to forest tent caterpillar (Malacosoma disstria) herbivory Planta 220 87–96

    Google Scholar 

  • L. Wilkinson (2000) SYSTAT: The System for Statistics SYSTAT, Inc. Evanston, IL

    Google Scholar 

  • J. Zheng M. Cho A. D. Jones B. D. Hammock (1997) ArticleTitleEvidence of quinone metabolites of naphthalene covalently bound to sulfur nucleophiles of proteins of murine clara cells after exposure to napthalene Chem. Res. Toxicol. 10 1008–1014

    Google Scholar 

Download references

Acknowledgments

We thank Michael M. Martin for suggesting revisions to our manuscript, Juha-Pekka Salminen for analyzing phenolic compounds with HPLC-DAD, Bob McCron for providing insect eggs, and David Borneman, Brian Klatt, and Marvin Pettway for permission to use trees at Kuebler-Langford Park, the Matthaei Botanical Gardens, and the University of Michigan, respectively. This work was supported by NSF grant IBN-9974583 to RVB.

Author information

Authors and Affiliations

  1. Departments of Molecular, Cellular and Developmental Biology, Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, 48109-1048, USA

    Raymond Barbehenn, Susannah Cheek, Adrian Gasperut, Emma Lister & Rosalyn Maben

Authors
  1. Raymond Barbehenn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susannah Cheek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adrian Gasperut
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emma Lister
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rosalyn Maben
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Raymond Barbehenn.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barbehenn, R., Cheek, S., Gasperut, A. et al. 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 (2005). https://doi.org/10.1007/s10886-005-4242-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-005-4242-4

Key Words

Search

Navigation