Journal of Chemical Ecology

, Volume 16, Issue 1, pp 165–185 | Cite as

Lepidoptera and pyrrolizidine alkaloids Exemplification of complexity in chemical ecology

  • Michael Boppré


Pyrrolizidine alkaloids (PAs) are defensive secondary metabolites found in numerous plant groups. Various insects belonging to different orders have special requirements for these compounds and sequester them from such plants for their own defense and often as pheromone precursors. The fitness of these insects depends on PAs and, in some cases, PAs even act as regulators of androconial organ development. This article discusses selected behavioral, chemical, physiological, and phylogenetic aspects of insect-PA relationships, and raises questions about the complex interactions of the variety of PA-related adaptations as they occur among a diverse array of species. Although many superficial similarities are recognized, few generalizations can yet be drawn. However, insect-PA relationships not only exemplify basic features of chemical ecology but illustrate a multiplicity of aspects and adaptations, which we should expect to find in any thorough study of insect-plant relationship.

Key Words

Pyrrolizidine alkaloids pharmacophagy male pheromones chemical defense Lepidoptera Danainae Arctiidae Heliotropium Senecio Crotalaria 


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  1. Ackery, P.R., andVane-Wright, R.I. 1984. Milkweed Butterflies—Their Cladistics and Biology. British Museum (Natural History), London.Google Scholar
  2. Aplin, R.T., andRothschild, M. 1968. Poisonous alkaloids in the body tissues of the cinnabar moth (Callimorpha jacobaeae L.).Nature 219:747–748.Google Scholar
  3. Aplin, R.T., andRothschild, M. 1972. Poisonous alkaloids in the body tissues of the garden tiger moth (Arctia caja L.) and the cinnabar moth [Tyria (=Callimorpha) jacobaeae L.] (Lepidoptera), pp. 579–595,in A. de Vries and K. Kochva (eds.). Toxins of Animal and Plant Origin. Gordon & Breach, London.Google Scholar
  4. Aplin, R.T., Benn, M.H., andRothschild, M. 1968. Poisonous alkaloids in the body tissues of the cinnabar mothI (Callimorphajacobaeae L.).Nature 219:747–748.Google Scholar
  5. Bell, T.W., andMeinwald, J. 1986. Pheromones of two arctiid moths (Creatonotos transferts andC. gangis); chiral components from both sexes and achiral female components.J. Chem. Ecol. 12:385–409.Google Scholar
  6. Bell, T.W., Boppré M., Schneider, D., andMeinwald, J. 1984. Stereochemical course of pheromone biosynthesis in an arctiid moth (Creatonotos transiens).Experientia 40:713–714.Google Scholar
  7. Benn, M., Degrave, J., Gnanasunderam, C., andHutchins, R. 1979. Host-plant pyrrolizidine alkaloids inNyctemera annulate Boisduval: Their persistance through the life-cycle and transfer to a parasite.Experientia 35:731–732.Google Scholar
  8. Bentley, M.D., Leonard, D.E., Stoddard, W.F., andZalkow, L.H. 1984. Pyrrolizidine alkaloids as larval feeding deterrents for spruce budworm,Choristoneura fiimiferana (Lepidoptera: Tortricidae).Ann. Entomol. Soc. Am. 77:393–397.Google Scholar
  9. Bernays, E.A., andChapman, R.F. 1977. Deterrent chemicals as a basis of oligophagymLocusta migratoria.Ecol. Entomol. 2:1–18.Google Scholar
  10. Bernays, E.A., Edgar, I.A., andRothschild, M. 1977. Pyrrolizidine alkaloids sequestered and stored by the aposematic grasshopperZonocerus variegatus.J. Zool. (London) 182:85–87.Google Scholar
  11. Blum, M.S. 1981. Chemical Defenses of Arthropods. Academic Press, New York.Google Scholar
  12. Bogner, F., andBoppré, M. 1989. Single cell recordings reveal hydroxydanaidal as the volatile compound attracting insects to pyrrolizidine alkaloids.Entomol. Exp. Appl. 50:171–184.Google Scholar
  13. Boppré, M. 1981. Adult Lepidoptera “feeding” at witheredHeliotropium plants (Boraginaceae) in East Africa.Ecol. Entomol. 6:449–452.Google Scholar
  14. Boppré, M. 1983. Leaf-scratching—a specialized behavior of danaine butterflies (Lepidoptera) for gathering secondary plant substances.Oecologia (Berlin) 59:414–416.Google Scholar
  15. Boppré, M. 1984a. Chemically mediated interactions between butterflies.Symp. R. Entomol. Soc. London 11:259–275 (=The Biology of Butterflies, R.I. Vane-Wright and P.R. Ackery (eds.). Academic Press, London).Google Scholar
  16. Boppré, M. 1984b. Redefining “pharmacophagy.”J. Chem. Ecol. 10:1151–1154.Google Scholar
  17. Boppré, M. 1986. Insects pharmacophagously utilizing defensive plant chemicals (pyrrolizidine alkaloids).Naturwissenschaften 73:17–26.Google Scholar
  18. Boppré, M., andPitkin, B.P. 1988. Attraction of chloropid flies to pyrrolizidine alkaloids (Diptera: Chloropidae).Entomol. Gener. 13:81–85.Google Scholar
  19. Boppré, M., andSchneider, D. 1985. Pyrrolizidine alkaloids quantitatively regulate both scent organ morphogenesis and pheromone biosynthesis in maleCreatonotos moths (Lepidoptera: Arctiidae).J. Comp. Physiol. 157:569–577.Google Scholar
  20. Boppré, M., andSchneider, D. 1989. On the biology ofCreatonotos (Lep.: Arctiidae) with special reference to the androconial system.Zool. J. Linn. Soc. 96:339–356.Google Scholar
  21. Boppré, M., Petty, R.L., Schneider, D., andMeinwald, J. 1978. Behaviorally mediated contacts between scent organs: another prerequisite for pheromone production inDanaus chrysippus males (Lepidoptera).J. Comp. Physiol. 126:97–103.Google Scholar
  22. Boppré, M., Seiet, U., andWickler, W. 1984. Pharmacophagy in grasshoppers?Zonocerus being attracted to and ingesting pure pyrrolizidine alkaloids.Entomol. Exp. Appl. 35:115–117.Google Scholar
  23. Borden J.H. 1985. Aggregation pheromones, pp. 257–285,in G.A. Kerkut and L.I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology 9. Pergamon Press, Oxford.Google Scholar
  24. Brower, L.P. 1969. Ecological chemistry.Sci. Am. 220(2):22–29.Google Scholar
  25. Brower, L.P. 1984. Chemical defence in butterflies.Symp. R. Entomol. Soc. London 11:109–134 (=The Biology of Butterflies, R.I. Vane-Wright and P.R. Ackery (eds.)). Academic Press, London.Google Scholar
  26. Brown, K.S. 1984a. Adult-obtained pyrrolizidine alkaloids defend ithomiine butterflies against a spider predator.Nature 309:707–709.Google Scholar
  27. Brown, K.S. 1984b. Chemical ecology of dehydropyrrolizine alkaloids in adult Ithomiinae (Lepidoptera: Nymphalidae).Rev. Brasil. Biol. 44:435–460.Google Scholar
  28. Brown, K.S. 1987. Chemistry at the Solanaceae/Ithomiinae interface.Ann, M. Bot. Gard. 74:359–397.Google Scholar
  29. Bull, L.B., Culvenor, C.C.J., andDick, A.T. 1968. The Pyrrolizidine Alkaloids. North-Holland Publ., Amsterdam.Google Scholar
  30. Conner, W.E., Eisner, T., Vandermeer, R.K., Guerrero, A., andMeinwald, J. 1981. Precopulatory sexual interaction in an archtiid moth (Utetheisa ornatrix): Role of a pheromone derived from dietary alkaloids.Behav. Ecol. Sociobiol. 9:227–235.Google Scholar
  31. Conner, W.E.,Roach, B.,Benedict, E.,Meinwald, J., andEisner, T. 1989. Courtship pheromone production and body size as correlates of larval diet in males of the arctiid moth,Utetheisa ornatrix. J. Chem. Ecol. In press.Google Scholar
  32. Culvenor, C.C.J., andEdgar, J.A. 1972. Dihydropyrrolizine secretions associated with coremata ofUtetheisa moths (family Arctiidae).Experientia 28:627–628.Google Scholar
  33. Culvenor, C.C.J., Edgar, J.A., andSmith, L.W. 1981. Pyrrolizidine alkaloids in honey fromEchium plantagineum L.J. Agric. Food Chem. 29:958–960.Google Scholar
  34. Devries, P.J., andStiles, F.G. 1989. Attraction of pyrrolizidine akaloids seeking Lepidoptera toEpidendrum paniculatum orchids and the potential effects of gene flow.Biotropica In press.Google Scholar
  35. Deinzer, M.L., Thomson, P.A., Burgett, D.M., andIsaacson, D.L. 1977. Pyrrolizidine alkaloids: their occurrence in honey from tansy ragwort (Senecio jacobaea L.).Science 195:497–499.Google Scholar
  36. Dussourd, D.E., Ubik, K., Harvis, K., Resch, J.F., Meinwald, J., andEisner, T. 1988. Biparental defensive endowment of eggs with acquired plant alkaloid in the mothUtethesia ornatrix.Proc. Natl. Acad. Sci. U.S.A. 85:5992–5996.Google Scholar
  37. Edgar, J. A., Culvenor, C.C.J., andPliske, T.E. 1976. Isolation of a lactone, structurally related to the esterifying acids of pyrrolizidine alkaloid' from the costal fringes of male Ithomiinae.J. Chem. Ecol. 2:263–270.Google Scholar
  38. Edgar, J.A., Culvenor, C.C.J., Cockrum, P.A., Smith, L.W., andRothschild, M. 1980. Callimorphine: identification and synthesis of the cinnabar moth “metabolite.”Tetrahedron Lett. 21:1383–1384.Google Scholar
  39. Ehmke, A., Proksch, P., Witte, L., Hartmann, T., andIsman, M.B. 1989. Fate of ingested pyrrolizidine alkaloid A'-oxide in the grasshopperMelanoplus sanguinipes.Naturwissenschaften 76:27–29.Google Scholar
  40. Eisner, T. 1980. Chemistry, defence, and survival: Case studies and selected topics, pp. 847–878,in M. Locke and D.S. Smith (eds.). Insect Biology in the Future. Academic Press, London.Google Scholar
  41. Eisner, T. 1982. For love of nature: Exploration and discovery at biological field stations.Bio-Science 32:321–326.Google Scholar
  42. Eisner, T., andMeinwald, J. 1987. Alkaloid-derived pheromones and sexual selection in Lepidoptera, pp. 251–269,in G.D. Prestwich and G.J. Blomquist (eds.). Pheromone Biochemistry. Academic Press, Orlando, Florida.Google Scholar
  43. Goss, G.J. 1979. The interaction between moths and plants containing pyrrolizidine alkaloids.Environm. Entomol. 8:487–493.Google Scholar
  44. Goss, G.J., andAdams, R.M. 1976. The reproductive biology of the epiphytic orchids of Florida IV. Sexually selective attraction of moths to the floral fragrance ofEpidendrum anceps Jacquin.Am. Orchid Soc. Bull. 45:997–1001.Google Scholar
  45. Haber, W.A. 1978. Evolutionary Ecology of Tropical Mimetic Butterflies. PhD thesis. University of Minnesota.Google Scholar
  46. Hartmann, T. 1985. Prinzipien des pflanzlichen Sekundärstoffwechsels.Plant Syst. Evol. 150:15–34.Google Scholar
  47. Hartmann, T., andToppel, G. 1987. Senecionine N-oxide, the primary product of pyrrolizidine alkaloid biosynthesis in root cultures ofSenecio vulgaris.Phytochemistry 26:1639–1643.Google Scholar
  48. Hartmann, T., Sander, H., Adolph, R., andToppel, G. 1988. Metabolic links between the biosynthesis of pyrrolizidine alkaloids and polyamines in root cultures ofSenecio vulgaris.Planta 175:82–90.Google Scholar
  49. Johnson, A.E., andMolyneux, R.J. 1985. Variation in toxic pyrrolizidine alkaloid content of plants, associated with site, stage of growth and environmental conditions, pp. 209–218, in A.A. Seawright, M.P. Hegarty, L.F. James, and R.F. Keller (eds.). Plant Toxicology. Yeerongpilly, Australia.Google Scholar
  50. Kelley, R.B., Seiber, J.N., Jones, A.D., Segall, H.J., andBrower, L.P. 1987. Pyrrolizidine alkaloids in overwintering monarch butterflies (Danaus plexippus) from Mexico.Experientia 43:943–946.Google Scholar
  51. Krasnoff, S.B., andDussourd, D.E. 1989. Dihydropyrrolizine attractants for arctiid moths that visit plants containing pyrrolizidine alkaloids,J. Chem. Ecol. 15:47–60.Google Scholar
  52. Krasnoff, S.B., andRoelofs, W.L. 1989. Quantitative and qualitative effects of larval diet on male scent secretions ofEstigmene acrea, Phragmatobia fuliginosa, andPyrrharctia Isabella (Lepidoptera: Arctiidae).J. Chem. Ecol. 15:1077–1093.Google Scholar
  53. Krasnoff, S.B., Bjostad, L.B., andRoelofs, W.L. 1987. Quantitative and qualitative variation cin male pheromones ofPhragmatobia fuliginosa andPyrrharctia Isabella (Lepidoptera: Arctiidae).J. Chem. Ecol., 13:807–822.Google Scholar
  54. L'empereur, K.M., Li, Y., Stermitz, F.R., andCrabtree, L. 1989. Pyrrolizidine alkaloids fromHackelia californien andGnophaela latipennis, andH. californica-hosted arctiid moth.J. Nat. Prod. 52:360–366.Google Scholar
  55. Malcolm, S., andRothschild, M. 1983. A danaid Müllerian mimic,Euploea core amymone (Cramer) lacking cardenolides in the pupal and adult stages.Biol. J. Linn. Soc. 19:27–33.Google Scholar
  56. Mattocks, A.R. 1986. Chemistry and Toxicology of Pyrrolizidine Alkaloids. Academic Press, London.Google Scholar
  57. Molyneux, R.J., andJohnson, A.E. 1984. Extraordinary levels of production of pyrrolizidine alkaloids inSenecio riddellii.J. Nat. Prod. 47:1030–1032.Google Scholar
  58. Mustaparta, H. 1984. Olfaction, pp. 37–70,in J.W. Bell and R.T. Cardé (eds.). Chemical Ecology of Insects. Chapman and Hall, London.Google Scholar
  59. Pliske, T.E. 1975a. Attraction of Lepidoptera to plants containing pyrrolizidine alkaloids.Environm. Entomol. 4:455–473.Google Scholar
  60. Pliske, T.E. 1975b. Pollination of pyrrolizidine alkaloid-containing plants by male Lepidoptera.Environm. Entomol. 4:475–479.Google Scholar
  61. Pliske, T.E., Edgar, J.A., andCulvenor, C.C.J. 1976. The chemical basis of attraction of ithomiine butterflies to plants containing pyrrolizidine alkaloids.J. Chem. Ecol. 2:255–262.Google Scholar
  62. Robins, D.J. 1982. The pyrrolizidine alkaloids.Progr. Chem. Nat. Prod. 41:115–203.Google Scholar
  63. Rothschild, M. 1985. British aposematic Lepidoptera, pp. 9–62,in J. Heath (ed.). The Moth and Butterflies of Great Britain and Ireland, Vol. 2. Harley Books, Colchester, U.K.Google Scholar
  64. Rothschild, M., van Euw, J., Aplin, R., andHarman, R.R.M. 1970. Toxic Lepidoptera.Taxicon 8:293–299.Google Scholar
  65. Rothschild, M., Aplin, R.T., Cockrum, P.A., Edgar, J.A., Fairweather, P., andLees, R. 1979. Pyrrolizidine alkaloids in arctiid moths (Lep.) with a discussion on host plant relationships and the role of these secondary plant substances in the Arctiidae.Biol. J. Linn. Soc. 12:305–326.Google Scholar
  66. Scherer, G., andBoppré, M. 1990. Attraction ofGabonia andNzerekorena (Chrysomelidae, Alticinae) to pyrrolizidine alkaloids—with descriptions of 13 new species and notes on male structural peculiarities.J. Nat. Hist. Submitted.Google Scholar
  67. Schneider, D. 1987. The strange fate of pyrrolizidine alkaloids, pp. 123–143,in R.F. Chapman, E.A. Bernays, and J.G. Stoffolano (eds.). Perspectives in Chemoreception and Behavior. Springer Verlag, Heidelberg.Google Scholar
  68. Schneider, D., Boppré, M., Zweig, J., Horsley, S.B., Bell, T.W., Meinwald, J., Hansen, K., andDiehl, E.W. 1982. Scent organ development inCreatonotos moths: Regulation by pyrrolizidine alkaloids.Science 215:1264–1265.Google Scholar
  69. Schulz, S. 1987. Die Chemie der Duftorgane männlicher Lepidopteren. Dissertation, Fachbereich Chemie der Universität Hamburg.Google Scholar
  70. Schulz, S., Francke, W., Edgar, J.A., andSchneider, D. 1988. Volatile compounds from androconial organs of danaine and ithomiine butterflies.Z. Naturforsch. 43c:99–104.Google Scholar
  71. Smith, L.W., andCulvenor, C.C.J. 1980. Plant sources of hepatotoxic pyrrolizidine alkaloids.J. Nat. Prod. 44:129–152.Google Scholar
  72. Toppel, G., Witte, L., andHartmann, T. 1988. N-Oxidation and degradation of pyrrolizidine alkaloids during germination ofCrotalaria scassellatii.Phytochemistry 27:3757–3760.Google Scholar
  73. Wiedenfeld, H. 1982. Two pyrrolizidine alkaloids fromGynura scandens.Phytochemistry 21:2767–2768.Google Scholar
  74. Wink, M., andSchneider, D. 1988. Carrier-mediated uptake of pyrrolizidine alkaloids in larvae of the aposematic and alkaloid-exploiting mothCreatonotos.Naturwissenschaften 75:524–525.Google Scholar
  75. Wink, M., Schneider, D., andWitte, L. 1988. Biosynthesis of pyrrolizidine alkaloid-derived pheromones in the arctiid moth,Creatonotos transiens: Stereochemical conversion of heliotrine.Z. Naturforsch. 43c:737–741.Google Scholar
  76. Wróbel, J.T. 1985. Pyrrolizidine alkaloids, pp. 327–384,in A. Brossi (ed.). The Alkaloids. Chemistry and Pharmacology, vol. 26. Academic Press, Orlando, Florida.Google Scholar
  77. Wunderer, H., Hansen, K., Bell, T.W., Schneider, D., andMeinwald, J. 1986. Male and female pheromones in the behavior of two Asian moths,Creatonotos (Lepidoptera: Arctiidae).Exp. Biol. 46:11–27.Google Scholar

Copyright information

© Plenum Publishing Corporation 1990

Authors and Affiliations

  • Michael Boppré
    • 1
  1. 1.Forstzoologisches Institut der Universität FreiburgStegen-WittentalGermany

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