Abstract
The potential interactions among a plant-produced allelochemical, a phytophagous insect, and an endotoxin produced byBacillus thuringiensis were investigated using purified cotton condensed tannins, the CryIA(c)δ-endotoxin fromB. thuringiensis subsp.kurstaki strain HD-73, and larvae ofHeliothis virescens. Purified condensed tannin from cotton fed to neonateH. virescens reduced feeding and mortality caused by insecticidal crystals ofB. thuringiensis. In fifth instars, tannin reduced relative growth rate (RGR), relative consumption rate (RCR), but antagonized the effects of the crystalδ-endotoxin. Tannin did not deter feeding of fifth instars in choice tests with cellulose-ester disks. Masking tannin from interacting with the dietary ingredients of artificial diets and crystal protein by encapsulation in alginate gel suggested that tannin adversely affected feeding after ingestion.These results suggest that insect control tactics that employδ-endotoxins in microbial insecticides and transgenic cotton plants may not be compatible when used in conjunction with plants containing high tannin concentrations.
Similar content being viewed by others
References
Adang, M.J., Staver, M.J., Rocheleau, T.A., Leighton, J., Barker, R.F., andThompson, D.V. 1985. Characterized full-length and truncated plasmid clones of the crystal protein ofBacillus thuringiensis subsp.kurstaki HD-73 and their toxicity toManduca sexta.Gene 36:289–300.
Barbosa, P., Krischik, V.A., andJones, C.G. (eds.) 1991. Microbial Mediation of Plant-Herbivore Interactions. John Wiley & Sons, New York.
Berenbaum, M.R. 1988. Allelochemicals in insect-microbe-plant interactions: Agents provocateurs in coevolutionary arms race, pp. 97–123,in P. Barbosa and D.K. Letourneau (eds.). Novel Aspects of Insect-Plant Interactions. Wiley-Interscience, New York.
Bernays, E.A., Cooper-Driver, G.C., andBilgener, M. 1989. Herbivores and plant tannins—a review.Adv. Ecol. Res. 19:263–302.
Chan, B.G., Waiss, A.C., Jr., andLukefahr, M. 1978. Condensed tannin: an antibiotic chemical fromGossypium hirsutum.J. Insect Physiol. 24:113–118.
Felton, G.W., andDahlman, D.L. 1984. Allelochemical-induced stress: Effects ofl-canavanine on the pathogenicity ofBacillus thuringiensis inManduca sexta.J. Invert. Pathol. 44:187–191.
Fischhoff, D.A., Bowdisch, K.S., Perlak, F.J., Marrone, P.O., McCormick, S.H., Nieder-Meyer, J.G., Dean, D.A., Kusano-Kretzmer, K., Mayer, E.J., Rochester, D.E., Rogers, S.G., andFraley, R.T. 1987. Insect tolerant transgenic tomato plants.Bio/Technology 5:807–813.
Gill, S.S., Cowles, E.A., andPietrantonio, P.V. 1992. The mode of action ofBacillus thuringiensis endotoxins.Annu. Rev. Entomol. 37:615–636.
Goodman, N.S., Gottfried, R.J., andRogoff, M.H. 1967. Biphasic system for separation of spores and crystals ofBacillus thuringiensis.J. Bacteriol. 94:485.
Gould, F., Martinez-Ramirez, A., Andersen, A., Ferre, J., Silva, F., andMoar, W.J. 1992. Broad-spectrum resistance toBacillus thuringiensis toxins inHeliothis virescens.Proc. Natl. Acad. Sci. U.S.A. 89:7896–7900.
Hagermann, A.E., andButler, L.G. 1978. Protein precipitation method for the quantitative determination of tannins.J. Agric. Food Chem. 26:809–812.
Hedin, P.A., Jenkins, J.N., Collum, D.H., White, W.H., andParrot, W.L. 1983. Multiple factors in cotton contributing to resistance to the tobacco budworm,Heliothis virescens, pp. 347–365,in P.A. Hedin (ed.) Plant Resistance to Insects. ACS Symposium Series 208. American Chemical Society, Washington, D.C.
Hofte, H., andWhiteley, H.R. 1989. Insecticidal crystal proteins ofBacillus thuringiensis.Micro-biol. Rev. 53:242–255.
Ibarra, J.E., andFederici, B.A. 1986. Isolation of a relatively nontoxic 65-kilodalton protein inclusion from the parasporal body ofBacillus thuringiensis subsp.israelensis.J. Bacteriol. 165:527–533.
Klocke, J.A., andChan, B.G. 1982. Effects of cotton condensed tannin on feeding and digestion in the cotton pest,Heliothis zea.J. Insect Physiol. 28:911–915.
Krischik, V.A., Barbosa, P., andReichelderfer, C.F. 1988. Three trophic level interactions: allelochemicals,Manduca sexta (L.)., andBacillus thuringiensis var.kurstaki Berliner.Environ. Entomol. 17:476–482.
Lane, H.C., andSchuster, M.F. 1981. Condensed tannins of cotton leaves.Phytochemistry 20:425–427.
Ludlum, C.T., Felton, G.W., andDuffey, S.S. 1991. Plant defenses: chlorogenic acid and polyphenol oxidase enhance toxicity ofBacillus thuringiensis subsp.kurstaki toHeliothis zea. J. Chem. Ecol. 17:217–237.
Luthy, P., Hofmann, C., andJaquet, F. 1985. Inactivation of delta endotoxin ofBacillus thuringiensis by tannin.FEMS Microbiol. Lett. 28:3133.
Morris, O.N. 1974. Inhibitory effects of foliage extracts of some forest trees on commercialBacillus thuringiensis.Can. Entomol. 104:1357–1361.
Navon, A., Klein, M., andBraun, S. 1990.Bacillus thuringiensis potency bioassays againstHeliothis armigera, Earias insulana andSpodoptera littoralis larvae based on standardized diets.J. Invert. Pathol. 55:387–393.
Navon, A., Federici, B.A., andWalsh, T.S. 1992. Mandibular adduction force ofHeliothis virescens (Lepidoptera: Noctuidae) larvae fed the insecticidal crystals ofBacillus thuringiensis.J. Econ. Entomol. 85: 2138–2143.
Perlak, F.J., Deaton, R.W., Armstrong, T.A., Fuchs, R.L., Sims, S.R., Greenplate, J.T., andFischhoff, D.A. 1990. Insect resistant cotton plants.Bio/Technology 8:939–943.
Reichelderfer, C.F. 1991. Interactions among allelochemicals, some Lepidoptera, andBacillus thuringiensis Berliner, pp.507–524,in P. Barbosa, V.A. Krischik, and C.G. Jones (eds.). Microbial Mediation of Plant-Herbivore Interactions. John Wiley & Sons, New York.
SAS Institute. 1989. SAS User's Guide: Statistics. Version 6.06 ed. SAS Institute, Cary, North Carolina.
Schultz, J.C. 1989. Tannin-insect interactions, pp. 417–433,in R.W. Hemingway and J.J. Karchesy (eds.). Chemistry and Significance of Condensed Tannins. Plenum Press, New York.
Shorey, H.H., andHale, R.I. 1965. Mass rearing of the larvae of nine noctuid species on a simple artificial medium.J. Econ. Entomol. 58:522–524.
Smirnoff, W.A., andHutchinson, P.M. 1965. Bacteriostatic and bactericidal effects of extracts of foliage from various plant species onBacillus thuringiensis var.thuringiensis Berliner.J. Invert. Pathol. 7:273–280.
White, W.H., Jenkins, J.N., Parrott, W.L., McCarty, J.C., Jr., Collum, D.H., andHedin, P.A. 1982. Strain and within season variability of various allelochemics within a diverse group of cottons.Crop Sci. 22:1235–1238.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Navon, A., Hare, J.D. & Federici, B.A. Interactions amongHeliothis virescens larvae, cotton condensed tannin and the CryIA(c) δ-endotoxin ofBacillus thuringiensis . J Chem Ecol 19, 2485–2499 (1993). https://doi.org/10.1007/BF00980685
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00980685