Journal of Chemical Ecology

, Volume 17, Issue 9, pp 1821–1836 | Cite as

Reassessment of the role of gut alkalinity and detergency in insect herbivory

  • Gary W. Felton
  • Sean S. Duffey


Previously it was reported that significant amounts of the tomato phenolic, chlorogenic acid, were oxidized in the digestive system of generalist feedersSpodoplera exigua andHelicoverpa zea. The covalent binding of the oxidized phenolic (i.e., quinone) to dietary protein exerts a strong antinutritive effect against larvae. In this study, we examined the fate of ingested chlorogenic acid in larvalManduca sexta, a leaf-feeding specialist of solanaceous plants. Significant amounts of chlorogenic acid were bound to excreted protein byM. sexta when larvae fed on tomato foliage. However, in the case ofM. sexta we suggest that the strong alkalinity and detergency of the midgut may minimize the antinutritive effects of oxidized phenolics. The solubility of tomato leaf protein is significantly greater at pH 9.7, representative of the midgut ofM. sexta, than at pH 8.0, representative of the midguts ofH. zea and S. exigua. We suggest that this increase in solubility would compensate for any loss in bioavailability of essential amino acids caused by the covalent binding of chlorogenic acid to amino acids. Furthermore, lysolecithin, a surfactant likely to contribute to the detergent properties of the midgut fluid, was shown to enhance protein solubility as well as inhibit polyphenol oxidase activity. The adaptive significance of gut alkalinity and detergency is discussed.

Key Words

Manduca sexta Lycopersicon phenolics chlorogenic acid polyphenol oxidase midgut pH surfactants detergency alkalinity herbivore adaptations plant defense lysolecithin insect nutrition 


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  1. Appel, H.M. andMartin, M.M. 1990. Gut redox conditions in herbivorous lepidopteran larvae.J. Chem. Ecol. 16:3277–3290.Google Scholar
  2. Barbeau, W.E., andKinsella, J.E. 1983. Factors affecting the binding of chlorogenic acid to fraction 1 leaf protein.J. Agric. Food Chem. 31:993–998.Google Scholar
  3. Barbeau, W.E., andKinsella, J.E. 1985. Effects of free and bound chlorogenic acid on the in vitro digestibility of ribulose bisphosphate carboxylase from spinach.J. Food Sci. 50:1083–1100.Google Scholar
  4. Berenbaum, M. 1980. Adaptive significance of midgut pH in larval lepidoptera.Am. Nat. 115:138–146.Google Scholar
  5. Betschart, A., andKinsella, J.E. 1973. Extractability and solubility of leaf protein.J. Agric. Food Chem. 21:60–64.Google Scholar
  6. Blytt, H.J., Guscar, T.K., andButler, L.G. 1988. Antinutritional effects and ecological significance of dietary condensed tannins may not be due to binding and inhibiting digestive enzymes.J. Chem. Ecol. 14:1455–1465.Google Scholar
  7. Broadway, R.M., Duffey, S.S., Pearce, G., andRyan, C.A. 1986. Plant proteinase inhibitors: A defence against herbivorous insects?Entomol. Exp. Appl. 24:94–100.Google Scholar
  8. Brodbeck, B.V., andStrong, D.R. 1987. Amino acid nutrition of herbivorous insects and stress to host plants, pp. 347–364,in P. Barbosa and J.C. Schultz (eds.). Insect Outbreaks. Academic Press, New York.Google Scholar
  9. Chippendale, G.M. 1970. Metamorphic changes in fat body proteins of the southwestern corn borerDiatraea grandiosella.J. Insect Physiol. 16:1057–1068.Google Scholar
  10. Ciliers, J.J.L., andSingleton, V.L. 1989. Nonenzymic autoxidative phenolic browning reactions in a caffeic acid model system.J. Agric. Food Chem. 37:890–896.Google Scholar
  11. Dow, J.A.T. 1984. Extremely high pH in biological systems: a model for carbonate transport.Am. J. Physiol. 246R:633–635.Google Scholar
  12. Duffey, S.S., andFelton, G.W. 1989. Role of plant enzymes in resistance to insects, pp. 289–313,in J. Whitaker and P. Sonnet (eds.). Biocatalysis in Agricultural Biotechnology. American Chemical Society, Washington, D.C.Google Scholar
  13. Feeny, P.P. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars.Ecology 51:561–581.Google Scholar
  14. Felton, G.W., andDuffey, S.S. 1990. Inactivation of a baculovirus by quinones formed in insectdamaged plant tissues.J. Chem. Ecol. 16:1221–1236.Google Scholar
  15. Felton, G.W., Donato, K., Del Vecchio, R.J., andDuffey, S.S. 1989a. Activation of plant foliar oxidases by insect feeding reduces the nutritive quality of foliage for noctuid herbivores.J. Chem. Ecol. 15:2667–2694.Google Scholar
  16. Felton, G.W., Broadway, R.M., andDuffey, S.S. 1989b. Inactivation of protease inhibitors by plant-derived quinones: Complications for host-plant resistance against noctuid herbivores.J. Insect Physiol. 35:981–990.Google Scholar
  17. Finot, P.A. 1983. Influence of processing on the nutritional value of proteins.Qual. Plant Foods Hum. Nutr. 32:439–453.Google Scholar
  18. Friedman, M. 1982. Lysinoalanine formation in soybean proteins: Kinetics and mechanisms, pp. 231–273,in Food Protein Deterioration. Mechanisms and Functionality. J.P. Cherry (ed.). American Chemical Society, Washington, D.C.Google Scholar
  19. Fujita, S., andTono, T. 1988. Purification and some properties of polyphenol oxidase in eggplant (Solanum melongela).J. Sci. Food Agric. 46:115–123.Google Scholar
  20. Gentile, I.A., Ferraris, L., andMatta, A. 1988. Variations of polyphenoloxidase activities as a consequence of stresses that induce resistance toFusarium wilt of tomato.J. Phytopathol. 122:45–53.Google Scholar
  21. Hare, J.D. 1983. Manipulation of host suitability for herbivore pest management, pp. 655–680,in R.F. Denno and M.S. McClure (eds.). Variable Plants and Herbivores in Natural and Managed Systems. Academic Press, New York.Google Scholar
  22. Haslam, E. 1988. Plant polyphenols (syn. vegetable tannins) and chemical defense—a reappraisal.J. Chem. Ecol. 14:1789–1805.Google Scholar
  23. Hurrell, R.F., andFinot, P.A. 1985. Effects of food processing on protein digestibility and amino acid availability, pp. 233–246,in J.W. Finley and D.T. Hopkins (eds.). Digestibility and Amino Acid Availability in Cereals and Oilseeds. American Association of Cereal Chemists, St. Paul, Minnesota.Google Scholar
  24. Hurrell, R.F., Finot, P.A., andCuq, J.L. 1982. Protein-polyphenol reactions. 1. Nutritional and metabolic consequences of the reaction between oxidized caffeic acid and the lysine residues of casein.J. Nutr. 47:191–211.Google Scholar
  25. Igarashi, K., andYasui, T. 1985. Oxidation of free methionine and methionine residues in protein involved in the browning reaction of phenolic compounds.Agric. Biol. Chem. 49:2309–2315.Google Scholar
  26. Isman, M.B., andDuffey, S.S. 1983. Pharmacokinetics of chlorogenic acid and rutin in larvae ofHeliothis zea.J. Insect Physiol. 29:295–300.Google Scholar
  27. Jones, C.G., Hare, J.D., andCompton, S.J. 1989. Measuring plant protein with the Bradford assay. 1. Evaluation and standard method.J. Chem. Ecol. 15:979–992.Google Scholar
  28. Kalyanaraman, B., Premovic, P.I., andSealy, R.C. 1987. Semiquinone anion radicals from the addition of amino acids, peptides, and proteins to quinones derived from the oxidation of catechols and catecholamines.J. Biol. Chem. 262:11080–11087.Google Scholar
  29. Kang, K., Choo, Y., andKim, K. 1983. Enzymatic discoloration of raw potato tubers: With special reference to the formation and inhibition of dopachrome.Am. Potato J. 60:451–460.Google Scholar
  30. Lange, W.H., andBronson, L. 1981. Insect pests of tomato.Annu. Rev. Entomol. 26:345–371.Google Scholar
  31. Martin, J.S., andMartin, M.M. 1983. Tannin assays in ecological studies: Precipitation of ribulose-1,5-bisphosphate carboxylase/oxygenase by tannic acid, quebracho, and oak foliage extracts.J. Chem. Ecol. 9:285–294.Google Scholar
  32. Martin, J.S., Martin, M.M., andBernays, E.A. 1987. Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores.J. Chem. Ecol. 13:605–621.Google Scholar
  33. Martin, M.M., andMartin, J.S. 1984. Surfactants: Their role in preventing the precipitation of proteins by tannins in insect guts.Oecologia 61:342–345.Google Scholar
  34. Mattson, W.J. 1980. Herbivory in relation to nitrogen content.Annu. Rev. Ecol. Syst. 11:119–161.Google Scholar
  35. Mayer, A.M. 1987. Polyphenol oxidases in plants-recent progress.Phytochemistry 26:11–20.Google Scholar
  36. Mayer, A.M., andHarel, E. 1979. Polyphenol oxidases in plants.Phytochemistry 8:193–215.Google Scholar
  37. Meyer, H.-U., andBiehl, B. 1981. Activation of latent phenolase during spinach leaf senescence.Phytochemistry 20:955–959.Google Scholar
  38. Mole, S., andWaterman, P.G. 1985. Stimulatory effects of tannins and cholic acid on tryptic hydrolysis of proteins: Ecological implications.J. Chem. Ecol. 11:1323–1332.Google Scholar
  39. Pierpoint, W.S. 1983. Reactions of phenolic compounds with proteins, and their relevance to the production of leaf protein, pp. 235–267,in L. Telek and H.D. Graham, (eds.). Leaf Protein Concentrates. Avi Publ. Westport, Connecticut.Google Scholar
  40. Rock, G.C., andHodgson, E. 1971. Dietary amino acid requirements forHeliothis zea determined by dietary deletion and radiometric techniques.J. Insect Physiol. 17:1087–1097.Google Scholar
  41. Ryan, J.D., Gregory, P., andTingey, W.M. 1982. Phenolic oxidase activities in glandular trichomes ofSolanum berthaultii.Phytochemistry 21:1885–1887.Google Scholar
  42. Sandstrom, R.P., andCleland, R.E. 1989. Selective delipidation of plasma membrane by surfactants.Plant Physiol. 90:1524–1531.Google Scholar
  43. Sharma, R.C., andAli, R. 1980. Isolation and characterization of catechol oxidase fromSolanum melongena.Phytochemistry 19:1597–1600.Google Scholar
  44. Singer, S.J., Eggman, L., Campbell, J.M., andWildman, S.G. 1952. The proteins of green leaves. IV. A high molecular weight protein comprising a large part of the cytoplasmic proteins.J. Biol. Chem. 197:233–239.Google Scholar
  45. Terra, W.R. 1988. Physiology and biochemistry of insect digestion: An evolutionary perspective.Braz. J. Med. Biol. Res. 21:675–734.Google Scholar
  46. Whitaker, J.R., andFeeney, R.E. 1983. Chemical and physical modification of proteins by the hydroxide ion.CRC Crit. Rev. Food Sci. Nutr. 19:173–212.Google Scholar
  47. White, T.C.R. 1978. The importance of a relative shortage of food in animal ecology.Oecologia 33:71–86.Google Scholar
  48. Woodham, A.A. 1983. The nutritional evaluation of leaf protein concentrates, pp. 415–433,in L. Telek and H.D. Graham (eds.). Leaf Protein Concentrates. Avi Publ., Westport, Connecticut.Google Scholar
  49. Zucker, W.V. 1983. Tannins: does structure determine function? An ecological perspective.Am. Nat. 121:335–365.Google Scholar

Copyright information

© Plenum Publishing Corporation 1991

Authors and Affiliations

  • Gary W. Felton
    • 1
  • Sean S. Duffey
    • 1
  1. 1.Department of EntomologyUniversity of CaliforniaDavis
  2. 2.Department of EntomologyUniversity of ArkansasFayetteville

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