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Light-mediated allelochemical effects of naturally occurring polyacetylenes and thiophenes from asteraceae on herbivorous insects

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Abstract

Polyacetylenes and their thiophene derivatives, characteristic secondary metabolites of the Asteraceae, were examined for their effects on herbivorous insects. Three thiophenes (a monothiophene, a bithiophene, and α-terthienyl) and four polyacetylenes (phenylheptatriyne, phenylheptadiynene, phenylheptadiyene acetate, and matricaria lactone) were studied for their phototoxicity and light-independent toxicity to (1) a polyphagous lepidopteran,Ostrinia nubilalis, whose host range includes a number of phototoxic Asteraceae, (2) a polyphagous lepidoteran,Euxoa messoria, whose host range includes very few species of Asteraceae, and (3) an oligophagous lepidopteran,Manduca sexta, which is a specialist on Solanaceae. Several compounds were phototoxic toM. sexta andE. messoria even at very low irradiance levels, but behavioral adaptations, including spinning silk and boring into diet, allowedO. nubilalis to avoid photosensitization. Light-independent activity of the compounds to all three species involved feeding deterrence increasing in the orderO. nubilalis, E. messoria, andM. sexta, and longterm metabolic toxicity in the form of impaired nutrient utilization. The biosynthetically derived thiophenes were more toxic than their acetylenic precursors, and toxicity increased with increasing number of thiophene rings. The results are discussed in terms of plant-insect coevolution.

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References

  • Arnason, T., Chan, G.F.Q., Downum, C.-K., andTowers, G.H.N. 1981a. Oxygen requirement for near-UV mediated cytotoxicity of α-terthienyl toEscherichia coli andSaccharomyces cerevisia.Photochem. Photobiol. 33:821–824.

    Google Scholar 

  • Arnason, T., Stein, J.R., Graham, E., Wat, C.-K., Towers, G.H.N., andLam, J. 1981b. Phototoxicity to selected marine and fresh-water algae of polyacetylenes from species in the Asteraceae.Can. J. Bot. 59:54–58.

    Google Scholar 

  • Arnason, T., Swain, T., Wat, C.-K., Graham, E., Partington, S., Towers, G.H.N., andLam, J. 1981c. Mosquito larvicidal activity of polyacetylenes from species in the Asteraceae.Biochem. Syst. Ecol. 9:63–68.

    Google Scholar 

  • Arnason, T., Towers, G.H.N., Philogène, B.J.R., andLambert, J. 1983a. The role of natural photosensitizers in plant resistant to insects, pp. 139–151,in P. Hedin (ed.). Plant Resistance to Insects. ACS Symposium Series 208. ACS, Washington, D.C.

    Google Scholar 

  • Arnason, T., Morand, P., Salvador, J., Reyes, I., Lambert, J., andTowers, G.H.N. 1983b. Phototoxic substances fromFlaveria trinervis andSimira salvadorensis.Phytochemistry 22:594–595.

    Google Scholar 

  • Bakker, J., Gommers, F.J., Nieuwenhuis, I., andWynberg, H. 1979. Photoactivation of the nematocidal compound α-terthienyl from roots of marigolds (Tagetes species).J. Biol. Chem. 254:1841–1844.

    Google Scholar 

  • Beck, S.D., andReese, J.C. 1976. Insect-plant interactions: Nutrition and metabolism.Recent Adv. Phytochem. 10:41–92.

    Google Scholar 

  • Berenbaum, M. 1978. Toxicity of a furanocoumarin to armyworms: A case of biosynthetic escape from insect herbivores.Science 201:532–534.

    Google Scholar 

  • Berenbaum, M. 1981. Patterns of furanocoumarin distribution and insect herbivory in the Umbelliferae: Plant chemistry and community structure.Ecology 62:1254–1266.

    Google Scholar 

  • Berenbaum, M. 1983. Coumarins and caterpillars: A case for coevolution.Evolution 37:163.

    Google Scholar 

  • Berenbaum, M., Feeny, P. 1981. Toxicity of angular furanocoumarins to swallowtail butterflies: Escalation in an coevolutionary arms race?Science 212:927–929.

    Google Scholar 

  • Binder, R.G., Chan, B.G. 1982. Effects of cyclopropanoid and cyclopropanoid fatty acids on growth of pink bollworm, bollworm, and tobacco budworm.Entomol. Exp. Appl. 31:291–295.

    Google Scholar 

  • Binder, R.G., Chan, B.G., Elliger, C.A. 1979. Antibiotic effects of C10–C12 fatty acid esters on pink bollworm, bollworm, anf tobacco budworm.Agric. Biol. Chem. 43:2467–2471.

    Google Scholar 

  • Bohlmann, F., Burkhardt, T., andZdero, C. 1973. Naturally Occurring Acetylenes. Academic Press, N.Y., 547 pp.

    Google Scholar 

  • Bourque, G. 1984. Photosensitization ofFusarium culmorum by phenylheptatriyne from the Asteraceae. MSc thesis, University of Ottawa. 112 pp.

  • Broome, J.R., Callaham, M.F., Poe, W.E., andHeitz, J.R. 1975. Biochemical changes in the boll weevil induced by rose bengal in the absence of light.Chem. Biol. Interact. 14:203–206.

    Google Scholar 

  • Burnett, Jr., W.C., Jones, Jr., S.B., Mabry, T.J., andPadolina, W.G. 1974. Sesquiterpene lactones: Insect feeding deterrents inVeronia.Biochem. Syst. Ecol. 2:25–29.

    Google Scholar 

  • Caffrey, D.J., andWorthley, L.H. 1927. A progress report on the investigations of the European corn borer. USDA Dept. Bull. 1476. 155 pp.

  • Callaham, M.F., Lewis, L.A., Holloman, M.E., Broome, J.R., andHeitz, J.R. 1975. Inhibition of the acetylcholinesterase from the imported fire ant,Solenopsis richten (Forel), by dye-sensitized photooxidation.Comp. Biochem. Physiol. 51C:123–128.

    Google Scholar 

  • Callaham, M.F., Broome, J.R., Poe, W.E., Heitz, J.R. 1977a. Time dependance of light-independent biochemical changes in the boll weevil,Anthonomus grandis, caused by dietary rose bengal.Environ. Entomol. 6:669–673.

    Google Scholar 

  • Callaham, M.F., Palmertree, C. O., Broome, J.R., andHeitz, J.R. 1977b. Dye-sensitized photoinactivation of the lactic dehydrogenase and acetyl cholinesterase from the boll weevil,Anthonomus grandis.Pest. Biochem. Physiol. 7:21–27.

    Google Scholar 

  • Campbell, G., Lambert, J.D.H., Arnason, T., andTowers, G.H.N. 1982. Allelopathic properties of α-terthienyl and phenylheptatriyne, naturally occurring compounds from the Asteraceae.J. Chem. Ecol. 8:961–972.

    Google Scholar 

  • Champagne, D.E., Arnason, J.T., Philogène, B.J.R., Campbell, G., andMcLachlan, D. 1984. Photosensitization and feeding deterrence ofEuxoa messoria by α-terthienyl a naturally occurring thiophene from the Asteraceae.Experientia 40:577–578.

    Google Scholar 

  • Chan, G.F.Q., Towers, G.H.N., andMitchell, J.C. 1975. Ultraviolet-mediated antibiotic activity of thiophene compounds ofTagetes.Phytochemistry 14:2295–2296.

    Google Scholar 

  • Clement, S.L., Schmidt, R.S., Szatmari-Goodman, G., andLevine, E. 1980. Activity of xanthene dyes against black cutworm larvae.J. Econ. Entomol. 73:390–392.

    Google Scholar 

  • Dahlman, D.L. 1977. Effect ofl-canavanine on the consumption and utilization of artificial diet by the tobacco hornworm,Manduca sexta.Entomol. Exp. Appl. 22:123–131.

    Google Scholar 

  • Devitt, B.D., Philogene, B.J.R., andHincks, C.F. 1980. Effects of veratrine, berberine, nicotine, and atropine on developmental characteristics and survival of the dark-sided cutwormEuxoa messoria (Lepidoptera: Noctuidae).Phytoprotection 61:88–102.

    Google Scholar 

  • Dewitt, P.J.G.M., andKeddie, E. 1981. Induction of polyacetylenic photoalexins inLycopersicon esculentum after inoculation withCladosporium fulvum (syn.Fulvia fulva).Physiol. Plant Pathol. 18:143–148.

    Google Scholar 

  • Downum, K.R., Hanncock, R.E.W., andTowers, G.H.N. 1982. Mode of action of α-terthienyl onEschrichia coli: Evidence for a photodynamic effect on membranes.Photochem. Photobiol. 36:517–532.

    Google Scholar 

  • Downum, K.R., Rosenthal, G.A., andTowers, G.H.N. 1984. Phototoxicity of the plant metabolite, α-terthienyl, to larvae ofManduca sexta (Sphingidae).Pest. Biochem. Physiol. 22:104–109.

    Google Scholar 

  • Eisner, T., Hill, D., Goetz, M., Jain, S., Alsop, D., Comazine, S., andMeinwald, J. 1981. Antifeedant action of (Z)-dihydromatricaria acid from soldier beetles (Chauliognathus spp.).J. Chem. Ecol. 7:1149–1157.

    Google Scholar 

  • Gommers, F.J., andGeerligs, J.W.G. 1973. Lethal effect of near-ultraviolet light onPratylenchus penetrans from roots ofTagetes.Nematologica 19:389–393.

    Google Scholar 

  • Graham, K., Graham, E.A., andTowers, G.H.N. 1980. Cercaricidal activity of phenylheptatriyne and α-terthienyl, naturally occurring compounds in species of the Asteraceae (Compositae).Can. J. Zool. 58:1955–1958.

    Google Scholar 

  • Guthrie, W.D. 1971. Resistance of maize to second brood European corn borders, pp. 165–179,in Report, of the 26th Annual Corn Sorghum Research Conference American Seed Association Publication 26.

  • Isman, M.B., andDuffey, S.S. 1982. Toxicity of tomato phenolic compounds to the fruitworm,Heliothis zea.Entomol Exp. Appl. 31:370–376.

    Google Scholar 

  • Isman, M.B., andRodriguez, E. 1983. Larval growth inhibitors from species ofParthenium (Asteraceae).Phytochemistry 22:2709–2713.

    Google Scholar 

  • Jermy, T. 1983. Multiplicity of insect antifeedants in plants, pp. 223–236, in D.L. Whitehead and W.S. Bowers (eds.). Current Themes in Tropical Ecology, Vol. 2. Natural Products for Innovative Pest Management. Pergamon Press, New York.

    Google Scholar 

  • Jermy, T., Butts, B.A., andMcDonough, L. 1981. Antifeedants for Colorado potato beetle I: Antifeeding constituents of some plants from the sagebrush community.Insect Sci. Appl. 1:237–242.

    Google Scholar 

  • Kagan, J., Beny, J.P., Chan, G., Dhawan, S.N., Jaworski, J.A., Kagan, E.D., Kessner, P.D., Murphy, M., andRogers, J.A. 1983. The phototoxicity of some 1.3-butadrines and related thiophenes against larvae of the mosquitoAedes aegypti.Insect. Sci. Appl. 4:377–381.

    Google Scholar 

  • Lavialle, M. 1983. Photodynamic action in two insects, the European cabbage butterfly,Pieris brassicae (L.) and the green aphid,Myzus persicae (Sulzer).Sonderdruck aus Bd. 95:133–140.

    Google Scholar 

  • Mabry, T.J., andGill, J.E. 1979. Sesquiterpene lactones and other terpenoids, pp. 502–538,in G.A, Rosenthal and D.H. Janzen (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York.

    Google Scholar 

  • McLachlan, D., Arnason, T., Philogène, B.J.R., Champagne, D. 1982. Antifeedant activity of the polyacetylene phenylheptatriyne (PHT), from the Asteraceae toEuxoa messoria (Lepidoptera: Noctuidae).Experientia 38:1061–1062.

    Google Scholar 

  • McLachlan, D., Arnason, T., andLam, J. 1984. The role of oxygen in photosensitization with polyacetylenes and thiophene derivatives.Photochem. Photobiol. 39:177–182.

    Google Scholar 

  • Philogene, B.J.R., Arnason, J.T., Berg, C.W., Duval, F., Champagne, D., Taylor, R.G., Leitch, L., andMorand, P. 1985. Synthesis and evaluation of the naturally occurring phototoxin, alpha-terthienyl, as a control agent for larvae ofaedes intrudens, Aedes atropalpus (Diptera: Culicidae) and ofSimulium verecundum (Diptera: Simuliidae).J. Econ. Entomol. 78:121–126.

    Google Scholar 

  • Puritch, G.S. 1975. The toxic effects of fatty acids and their salts on the balsam wooly aphid,Adeiges piceae (Ratz.).Can. J. For. Res. 5:515–522.

    Google Scholar 

  • Reese, J.C. 1979. Interactions of allelochemicals with nutrients in herbivore food, p. 309–330,in G. A. Rosenthal and D.H. Janzen (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York.

    Google Scholar 

  • Reese, J.C., Chan, B.G., Malm, N.R., Waiss, A., 1981. Feeding sites of bollworm larvae on cotton.Environ. Entomol. 10:81–84.

    Google Scholar 

  • Robinson, T. 1980. The Organic Constituents of Higher Plants, 4th ed. Cordus Press, Amherst, Massachusetts.

    Google Scholar 

  • Schoonhoven, L.M. 1982. Biological aspects of antifeedants.Entomol. Exp. Appl. 31:57–69.

    Google Scholar 

  • Stewart, J.G., Philogène, B.J.R. 1983. Reproductive potential of laboratory rearedManduca sexta as effected by sex ratio.Can. Entomol. 115:295–298.

    Google Scholar 

  • Tauton, M.T., andKhan, S.M. 1978. Effects of fenitrothion and aminocarb, at doses giving low mortality, on surviving eggs and larvae of the Eucalypt-defoliating chrysomelid beetleParopsis atomaria 01. III Histological changes in treated larvae.Aust. J. Zool. 26:139–146.

    Google Scholar 

  • Towers, G.H.N. 1980. Photosensitizers from plants and their photodynamic action.Prog. Phytochem. 6:183–202.

    Google Scholar 

  • Towers, G.H.N., andWat, C.K., 1978. Biological activity of polyacetylenes.Rev. Latinoam. Quim. 9:162–170.

    Google Scholar 

  • Towers, G.H.N., Wat, C.K., Graham, E.A., Bandoni, R.J., Chan, G.F.Q., Mitchell, J.C., andLam, J. 1979. UV-mediated antibiotic activity of species of Compositae caused by polyacetylenic compounds.Lloydia 40:487–498.

    Google Scholar 

  • Towers, G.H.N.,Arnason, J.T.,Wat, C.K., andLambert, J.D.H. 1984. Method for controlling pests using naturally occurring conjugated polyacetylenes. Can. Pat. 1,173,743.

  • Waldbauer, G.P. 1968. The consumption and utilization of food by insects.Adv. Insect Physiol. 5:229–288.

    Google Scholar 

  • Wat, C.K., Biswas, R.K., Graham, E.A., Bohm, L., Towers, G.H.N., andWaygood, E.R. 1979. Ultraviolet-mediated cytotoxic activity of phenylheptatriyne fromBidens pilosa L.J. Nat. Prod. 42:103–111.

    Google Scholar 

  • Wat, C.K., MacRae, W.D., Yamamoto, E., Towers, G.H.N., andLam, J. 1980. Phototoxic effects of naturally occurring polyacetylenes and α-terthienyl on human erythrocytes.Photochem. Photobiol. 32:167–172.

    Google Scholar 

  • Wat, C.K., Prasad, S.K., Graham, E.A., Partington, S., Arnason, T., Towers, G.H.N., andLam, J. 1981. Photosensitization of invertebrates by natural polyacetylenes.Biochem. Syst. Ecol. 9:59–62.

    Google Scholar 

  • Yamamoto, E., Wat, C.K., MacRae, W.D., Towers, G.H.N., andChan, C.F.Q. 1979. Photoinactivation of human erythrocyte enzymes by α-terthienyl and phenylheptatriyne, naturally occurring compounds in the Asteraceae.FEES Lett. 107:134–136.

    Google Scholar 

  • Yoho, T.P., Butler, L., andWeaver, J.E. 1971. Photodynamic effect of light on dye-fed house flies: Preliminary observations of mortality.J. Econ. Enlomol. 64:972–973.

    Google Scholar 

  • Yoho, T.P., Weaver, J.E., andButler, L., 1973. Photodynamic action in insects. I. Levels of mortality in dye-fed light-exposed house flies.Environ. Entomol. 2:1092–1096.

    Google Scholar 

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  1. D. E. Champagne

    Present address: Botany Department, University of British Columbia, V6T 1W5, Vancouver, British Columbia, Canada

Authors and Affiliations

  1. Ottawa Carleton Centre for Graduate Studies and Research in Biology and Chemistry, University of Ottawa, K1N 6N5, Ottawa, Ontario, Canada

    D. E. Champagne, J. T. Arnason, B. J. R. Philogène & P. Morand

  2. Department of Organic Chemistry, University of Aarhus, 8000, Aarhus, Denmark

    J. Lam

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  1. D. E. Champagne
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Champagne, D.E., Arnason, J.T., Philogène, B.J.R. et al. Light-mediated allelochemical effects of naturally occurring polyacetylenes and thiophenes from asteraceae on herbivorous insects. J Chem Ecol 12, 835–858 (1986). https://doi.org/10.1007/BF01020255

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