, Volume 159, Issue 4, pp 777–788 | Cite as

Tree resistance to Lymantria dispar caterpillars: importance and limitations of foliar tannin composition

  • Raymond V. Barbehenn
  • Adam Jaros
  • Grace Lee
  • Cara Mozola
  • Quentin Weir
  • Juha-Pekka Salminen
Plant-Animal Interactions - Original Paper


The ability of foliar tannins to increase plant resistance to herbivores is potentially determined by the composition of the tannins; hydrolyzable tannins are much more active as prooxidants in the guts of caterpillars than are condensed tannins. By manipulating the tannin compositions of two contrasting tree species, this work examined: (1) whether increased levels of hydrolyzable tannins increase the resistance of red oak (Quercus rubra L.), a tree with low resistance that produces mainly condensed tannins, and (2) whether increased levels of condensed tannins decrease the resistance of sugar maple (Acer saccharum Marsh.), a tree with relatively high resistance that produces high levels of hydrolyzable tannins. As expected, when Lymantria dispar L. caterpillars ingested oak leaves coated with hydrolyzable tannins, levels of hydrolyzable tannin oxidation increased in their midgut contents. However, increased tannin oxidation had no significant impact on oxidative stress in the surrounding midgut tissues. Although growth efficiencies were decreased by hydrolyzable tannins, growth rates remained unchanged, suggesting that additional hydrolyzable tannins are not sufficient to increase the resistance of oak. In larvae on condensed tannin-coated maple, no antioxidant effects were observed in the midgut, and levels of tannin oxidation remained high. Consequently, neither oxidative stress in midgut tissues nor larval performance were significantly affected by high levels of condensed tannins. Post hoc comparisons of physiological mechanisms related to tree resistance revealed that maple produced not only higher levels of oxidative stress in the midgut lumen and midgut tissues of L. dispar, but also decreased protein utilization efficiency compared with oak. Our results suggest that high levels of hydrolyzable tannins are important for producing oxidative stress, but increased tree resistance to caterpillars may require additional factors, such as those that produce nutritional stress.


Insect herbivore Induced defense Phenolics 


  1. Appel HM (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552CrossRefGoogle Scholar
  2. Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844PubMedCrossRefGoogle Scholar
  3. Ayres MP, Clausen TP, MacLean SF, Redman AM, Reichardt PB (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712Google Scholar
  4. Barbehenn RV (1995) Measurement of protein in whole plant samples with ninhydrin. J Sci Food Agric 69:353–359CrossRefGoogle Scholar
  5. Barbehenn RV, Martin MM (1994) Tannin sensitivity in Malacosoma disstria: roles of the peritrophic envelope and midgut oxidation. J Chem Ecol 20:1985–2001CrossRefGoogle Scholar
  6. Barbehenn RV, Walker AC, Uddin F (2003) Antioxidants in the midgut fluids of a tannin-tolerant and a tannin-sensitive caterpillar: effects of seasonal changes in tree leaves. J Chem Ecol 29:1099–1116PubMedCrossRefGoogle Scholar
  7. Barbehenn RV, Cheek S, Gasperut A, Lister E, Maben R (2005) Phenolic compounds in red oak and sugar maple leaves have prooxidant activities in the midguts of Malacosoma disstria and Orgyia leucostigma caterpillars. J Chem Ecol 31:969–988PubMedCrossRefGoogle Scholar
  8. Barbehenn RV, Jones CP, Karonen M, Salminen J-P (2006a) Tannin composition affects the oxidative activities of tree leaves. J Chem Ecol 32:2235–2251PubMedCrossRefGoogle Scholar
  9. Barbehenn RV, Jones CP, Hagerman AE, Karonen M, Salminen J-P (2006b) Ellagitannins have greater oxidative activities than gallotannins and condensed tannins at high pH: potential impact on caterpillars. J Chem Ecol 32:2253–2267PubMedCrossRefGoogle Scholar
  10. Barbehenn RV, Jones CP, Yip L, Tran L, Constabel CP (2007) Limited impact of elevated levels of polyphenol oxidase on tree-feeding caterpillars: assessing individual plant defenses with transgenic poplar. Oecologia 154:129–140PubMedCrossRefGoogle Scholar
  11. Barbehenn RV, Maben RE, Knoester JJ (2008a) Linking phenolic oxidation in the midgut lumen with oxidative stress in the midgut tissues of a tree-feeding caterpillar Malacosoma disstria (Lepidoptera: Lasiocampidae). Environ Entomol 37:1113–1118PubMedCrossRefGoogle Scholar
  12. Barbehenn RV, Weir Q, Salminen J-P (2008b) Oxidation of ingested phenolics in the tree-feeding caterpillar Orgyia leucostigma depends on foliar chemical composition. J Chem Ecol 34:748–756PubMedCrossRefGoogle Scholar
  13. Barbehenn RV, Jaros A, Lee G, Mozola C, Salminen J-P (2009) Hydrolyzable tannins as “quantitative defenses”: limited impact against Lymantria dispar caterpillars on hybrid poplar. J Insect Physiol (in press). doi:10.1016/j.jinsphys.2008.12.001
  14. Barbosa P, Krischik VA (1987) Influence of alkaloids on feeding preference of eastern deciduous forest trees by the gypsy moth Lymantria dispar. Am Nat 130:53–69CrossRefGoogle Scholar
  15. Berenbaum M (1983) Effects of tannin ingestion on two species of papilionid caterpillars. Entomol Exp Appl 34:245–250CrossRefGoogle Scholar
  16. Bernays EA, Chamberlain D, McCarthy P (1980) The differential effects of ingested tannic acid on different species of Acridoidea. Entomol Exp Appl 28:158–166CrossRefGoogle Scholar
  17. Bernays EA, Chamberlain DJ, Leather EM (1981) Tolerance of acridids to ingested condensed tannin. J Chem Ecol 7:247–256CrossRefGoogle Scholar
  18. 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 21:1511–1530CrossRefGoogle Scholar
  19. Buettner G (1993) The pecking order of free radicals and antioxidants: lipid peroxidation, α-tocopherol, and ascorbate. Arch Biochem Biophys 300:535–543PubMedCrossRefGoogle Scholar
  20. Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 102:19237–19242PubMedCrossRefGoogle Scholar
  21. Clausen TP, Pruenza FD, Burritt EA, Reichardt PB, Bryant JP (1990) Ecological implications of condensed tannin structure: a case study. J Chem Ecol 16:2381–2392CrossRefGoogle Scholar
  22. Farrar RR, Barbour JD, Kennedy GG (1989) Quantifying food consumption and growth in insects. Ann Entomol Soc Am 82:593–598Google Scholar
  23. Felton GW (1996) Nutritive quality of plant protein: sources of variation and insect herbivore responses. Arch Insect Biochem Physiol 32:107–130CrossRefGoogle Scholar
  24. Griffith O (1983) Glutathione and glutathione disulphide. Meth Enzym Anal 8:521–529Google Scholar
  25. Hagerman AE, Dean RT, Davies MJ (2003) Radical chemistry of epigallocatechin gallate and its relevance to protein damage. Arch Biochem Biophys 414:115–120PubMedCrossRefGoogle Scholar
  26. Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, New YorkGoogle Scholar
  27. Horton DR, Redak RA (1993) Further comments on analysis of covariance in insect dietary studies. Entomol Exp Appl 69:263–275CrossRefGoogle Scholar
  28. Hunter MD, Schultz JC (1993) Induced plant defenses breached? Phytochemical induction protects an herbivore from disease. Oecologia 94:195–203CrossRefGoogle Scholar
  29. Hunter MD, Schultz JC (1995) Fertilization mitigates chemical induction and herbivore responses within damaged oak species. Ecology 76:1226–1232CrossRefGoogle Scholar
  30. Kaitaniemi P, Ruohomaki K, Ossipov V, Haukioja E, Pihlaja K (1998) Delayed induced changes in the biochemical composition of host plant leaves during an insect outbreak. Oecologia 116:182–190CrossRefGoogle Scholar
  31. Karonen M, Loponen J, Ossipov V, Pihlaja K (2004) Analysis of procyanidins in pine bark with reversed-phase and normal-phase high-performance liquid chromatography–electrospray ionization mass spectrometry. Anal Chim Acta 522:105–112CrossRefGoogle Scholar
  32. Karowe DN (1989) Differential effect of tannic acid on two tree-feeding Lepidoptera: implications for theories of plant-herbivore chemistry. Oecologia 80:507–512CrossRefGoogle Scholar
  33. Kopper BJ, Jakobi VN, Osier TL, Lindroth RL (2002) Effects of paper birch condensed tannin on whitemarked tussock moth (Lepidoptera: Lymantriidae) performance. Environ Entomol 31:10–14Google Scholar
  34. Liebhold AM, Gottschalk KW, Muzika R-M, Montgomery ME, Young R, O’Day K, Kelley B (1995) Suitability of North American tree species to the gypsy moth: a summary of field and laboratory tests. United States Department of Agriculture Forest Service, Northeastern Forest Experimental Station, general technical report NE–211Google Scholar
  35. Manuwoto S, Scriber JM (1986) Effects of hydrolyzable and condensed tannin on growth and development of two species of polyphagous Lepidoptera: Spodoptera eridania and Callosamia promethea. Oecologia 69:225–230CrossRefGoogle Scholar
  36. Martin JS, Martin MM, Bernays EA (1987) Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: implications for theories of plant defense. J Chem Ecol 13:605–621CrossRefGoogle Scholar
  37. Moilanen J, Salminen J-P (2008) Ecologically neglected tannins and their biologically relevant activity: chemical structures of plant ellagitannins reveal their in vitro oxidative activity at high pH. Chemoecology 18:73–83CrossRefGoogle Scholar
  38. Nicol RW, Arnason JT, Helson B, Abou-Zaid MM (1997) Effect of host and non-host trees on the growth and development of the forest tent caterpillar, Malacosoma disstria Hübner (Lepidoptera: Lasiocampidae). Can Entomol 129:995–1003CrossRefGoogle Scholar
  39. Osier TL, Hwang SY, Lindroth RL (2000) Effects of phytochemical variation in quaking aspen Populus tremuloides clones on gypsy moth Lymantria dispar performance in the field and laboratory. Ecol Entomol 25:197–207CrossRefGoogle Scholar
  40. Parry D, Goyer RA (2004) Variation in the suitability of host tree species for geographically discrete populations of forest tent caterpillar. Environ Entomol 33:1477–1487Google Scholar
  41. Plymale R, Grove MJ, Cox-Foster D, Ostiguy N, Hoover K (2008) Plant-mediated alteration of the peritrophic matrix and baculovirus infection in lepidopteran larvae. J Insect Physiol 54:737–749PubMedCrossRefGoogle Scholar
  42. Raubenheimer D, Simpson SJ (1992) Analysis of covariance: an alternative to nutritional indices. Entomol Exp Appl 62:221–231CrossRefGoogle Scholar
  43. Roslin T, Salminen J-P (2008) Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species. Oikos 117:1560–1568CrossRefGoogle Scholar
  44. Rossiter M, Schulz JC, Baldwin IT (1988) Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology 69:267–277CrossRefGoogle Scholar
  45. Roth SK, Lindroth RL, Montgomery ME (1994) Effects of foliar phenolics and ascorbic acid on performance of the gypsy moth (Lymantria dispar). Biochem Syst Ecol 22:341–351CrossRefGoogle Scholar
  46. Salminen J-P, Lempa K (2002) Effects of hydrolysable tannins on a herbivorous insect: fate of individual tannins in insect digestive tract. Chemoecology 12:203–211CrossRefGoogle Scholar
  47. Salminen J-P, Roslin T, Karonen M, Sinkkonen J, Pihlaja K, Pulkkinen P (2004) Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J Chem Ecol 30:1693–1711PubMedCrossRefGoogle Scholar
  48. SAS Institute (2003) The SAS system for Windows. Version 9.1. SAS Institute, CaryGoogle Scholar
  49. Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151PubMedCrossRefGoogle Scholar
  50. Scriber JM (1978) The effects of larval feeding specialization and plant growth form on the consumption and utilization of plant biomass and nitrogen: an ecological consideration. Entomol Exp Appl 24:494–510CrossRefGoogle Scholar
  51. Steppuhn A, Baldwin IT (2007) Resistance management in a native plant: nicotine prevents herbivores from compensating for plant protease inhibitors. Ecol Lett 10:499–511PubMedCrossRefGoogle Scholar
  52. Swain T (1979) Tannins and lignins. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 657–682Google Scholar
  53. Van Soest PJ, Wine RH (1967) Use of detergents in the analysis of fibrous feeds. IV. Determination of plant cell-wall constituents. J Assoc Off Anal Chem 50:50–55Google Scholar
  54. Waldbauer GP (1968) The consumption and utilization of food by insects. Adv Insect Physiol 5:229–289CrossRefGoogle Scholar
  55. Wilkinson L (2000) SYSTAT: the system for statistics. SYSTAT, EvanstonGoogle Scholar
  56. Wold EN, Marquis RJ (1997) Induced defenses in white oak: effects on herbivores and consequences for the plant. Ecology 78:1356–1369CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Raymond V. Barbehenn
    • 1
  • Adam Jaros
    • 1
  • Grace Lee
    • 1
  • Cara Mozola
    • 1
  • Quentin Weir
    • 1
  • Juha-Pekka Salminen
    • 2
  1. 1.Departments of Molecular, Cellular and Developmental Biology and Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  2. 2.Laboratory of Organic Chemistry and Chemical Biology, Department of ChemistryUniversity of TurkuTurkuFinland

Personalised recommendations