Research Article

Journal of Chemical Ecology

, Volume 31, Issue 5, pp 969-988

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

  • Raymond BarbehennAffiliated withDepartments of Molecular, Cellular and Developmental Biology, Ecology and Evolutionary Biology, University of Michigan Email author 
  • , Susannah CheekAffiliated withDepartments of Molecular, Cellular and Developmental Biology, Ecology and Evolutionary Biology, University of Michigan
  • , Adrian GasperutAffiliated withDepartments of Molecular, Cellular and Developmental Biology, Ecology and Evolutionary Biology, University of Michigan
  • , Emma ListerAffiliated withDepartments of Molecular, Cellular and Developmental Biology, Ecology and Evolutionary Biology, University of Michigan
  • , Rosalyn MabenAffiliated withDepartments of Molecular, Cellular and Developmental Biology, Ecology and Evolutionary Biology, University of Michigan

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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.

Key Words

Prooxidant phenolic compound oxidation caterpillar Malacosoma disstria Orgyia leucostigma peroxide semiquinone radical protein carbonyl red oak Quercus rubra sugar maple Acer saccharum