Journal of Chemical Ecology

, Volume 7, Issue 6, pp 981–1010 | Cite as

Seasonal and intraplant variation of cardenolide content in the California milkweed,Asclepias eriocarpa, and implications for plant defense

  • C. J. Nelson
  • J. N. Seiber
  • L. P. Brower


Root, stem, leaf, and latex samples ofAsclepias eriocarpa collected from three plots in one population at 12 monthly intervals were assayed for total cardenolide content by spectroassay and for individual cardenolides by thin-layer chromatography. From May to September mean milligram equivalents of digitoxin per gram of dried plant were: latices, 56.8 ≫ stems, 6.12 > leaves, 4.0 > roots, 2.5. With the exception of the roots, significant changes in gross cardenolide content occurred for each sample type with time of collection during the growing season, whereas variation within this population was found to be small. Labriformin, a nitrogen-containing cardenolide of low polarity, predominated in the latices. Leaf samples contained labriformin, labriformidin, desglucosyrioside, and other unidentified cardenolides. In addition to most of the same cardenolides as the leaves, the stems also contained uzarigenin. The roots contained desglucosyrioside and several polar cardenolides. The results are compared with those for other cardenolide-containing plants, and discussed in relation to anti-herbivore defense based on plant cardenolide content. Arguments are advanced for a central role of the latex in cardenolide storage and deployment which maximizes the defensive qualities of the cardenolides while preventing toxicity to the plant.

Key words

Asclepias eriocarpa Asclepiadaceae milkweed cardenolides chemical defense chemical ecology labriformin labriformidin desglucosyrioside uzarigenin variation season plant part defense root stem leaf latex 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Barthakur, P. 1971. Programs 1324 EB/ST4 and 1326 EB/ST4, pages 6–8, 12–14, 700 Series Program Library, Vol. 9, Wang Laboratories, Inc., Tewkesbery, Massachusetts.Google Scholar
  2. Benson, J.M., Seiber, J.N., Keeler, R.F., andJohnson, A.E. 1978. Studies on the toxic principle ofAsclepias eriocarpa andAsclepias labriformis, pp. 273–284,in R.F. Keeler, K.R. van Kampen, and L.F. James (eds.). Effects of Poisonous Plants on Livestock. Academic Press, New York.Google Scholar
  3. Benson, J.M., Seiber, J.N., Bagley, C.V., Keeler, R.F., Johnson, A.E., andYoung, S. 1979. Effects on sheep of the milkweedsAsclepias eriocarpa andA. labriformis and of cardiac glycoside-containing derivative material.Toxicon 17:155–165.PubMedGoogle Scholar
  4. Brower, L.P. 1969. Ecological chemistry.Sci. Am. 220:22–29.PubMedGoogle Scholar
  5. Brower, L.P. 1970. Plant poisons in a terrestrial food chain and implications for mimicry theory, pp. 69–82,in K.L. Chambers (ed.). Proceedings of the 29th Annual Biological Colloquium, 1968, Biochemical Coevolution. Oregon State University Press, Corvallis.Google Scholar
  6. Brower, L.P., andGlazier, S.C. 1975. Localization of heart poisons in the monarch butterfly.Science 188:19–25.Google Scholar
  7. Brower, L.P., andHuberth, J.C. 1977. Strategy for Survival: Behavioral ecology of the monarch butterfly (motion picture film). Copyright 1977. (30 minutes, 16 mm, color cond.) Released by Harper and Row Media, September 1977, 2350 Virginia Ave., Hagerstown, Maryland 21740.Google Scholar
  8. Brower, L.P., McEvoy, P.B., Williamson, K.L., andFlannery, M.A. 1972. Variation in cardiac glycoside content of monarch butterflies from natural populations in eastern North America.Science 177:426–429.PubMedGoogle Scholar
  9. Brower, L.P., Edmunds, M., andMoffitt, C.M. 1975. Cardenolide content and palatability of a population ofDanaus chrysippus butterflies from West Africa.J. Entomol. (A)49:183–196.Google Scholar
  10. Brower, L.P.,Seiber, J.N.,Nelson, C.J.,Lynch, S.P., andTuskes, P.M. 1982. Plant determined variation in the cardenolide content, thin layer chromatography profiles, and emetic potency of monarch butterflies,Danaus plexippus reared on the milkweed,Asclepias eriocarpa in California.J. Chem. Ecol. In press.Google Scholar
  11. Brown, H.D., Neucere, N.J., Altschul, A.M., andEvans, W.J. 1965. Activity patterns of purified ATPase fromArachis hypogaea.Life Sci. 4:1439–1447.PubMedGoogle Scholar
  12. Brown, P., von Euw, J., Reichstein, T., Stöckel, K., andWatson, T.R. 1979. Cardenolides ofAsclepias syriaca L., probable structure of syrioside and syriobioside.Helv. Chim. Acta 62:412–441.Google Scholar
  13. Brüschweiler, F., Stocklin, W., Stöckel, K., andReichstein, T. 1969a. Die Glykoside vonCalotropis procera R. Br.Helv. Chim. Acta 52:2086–2106.PubMedGoogle Scholar
  14. Brüschweiler, F., Stöckel, K., andReichstein, T. 1969b.Calotropis glycoside, presumed partial structure,Helv. Chim. Acta 52:2276–2303.PubMedGoogle Scholar
  15. Cates, R.G. andRhoades, D.F. 1977. Patterns in the production of antiherbivore chemical defenses in plant communities.Biochem. Syst. Ecol. 5:185–193.Google Scholar
  16. Cheung, H.T., Watson, T.R., Seiber, J.N., andNelson, C.J. 1980. 7β,8β-Epoxy-cardenolide glycosides ofAsclepias eriocarpa.J. Chem. Soc. Perkin I. 1980:2169–2173.Google Scholar
  17. Daloze, D., andPasteels, J.M. 1979. Production of cardiac glycosides by chrysomelid beetles and larvae.J. Chem. Ecol. 5:63–77.Google Scholar
  18. Duffey, S.S., Blum, M.S., Isman, M.B., andScudder, G.G.E. 1978. Cardiac glycosides: A physical system for their sequestration by the milkweed bug.J. Insect Physiol. 24:639–645.Google Scholar
  19. Esau, K. 1965. Plant Anatomy, 2nd ed. Wiley & Sons, New York.Google Scholar
  20. Evans, F.J. 1977. A new phorbol triester from the latices ofEuphorbia frankiana andE. coerulescens.Phytochemistry 16:395–396.Google Scholar
  21. Evans, F.J., andCowley, P.S. 1972. Cardenolides and spirostanols inDigitalis purpurea at various stages of development.Phytochemistry 11:2971–2975.Google Scholar
  22. Evans, F.J., andSchmidt, R.J. 1976. Two new toxins from the latex ofEuphorbia poisonii.Phytochemistry 15:333–335.Google Scholar
  23. Euw, J. von, Fishelson, L., Parsons, J.A., Reichstein, T., andRothschild, M. 1967. Cardenolides (heart poisons) in a grasshopper feeding on milkweeds.Nature 214:35–39.PubMedGoogle Scholar
  24. Fairbairn, J.W., Hakim, F., andEl Kheir, Y. 1974. Alkaloidal storage, metabolism and translocation in the vesicles ofPapaver somniferum latex.Phytochemistry 13:1133–1139.Google Scholar
  25. Feeny, P. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars.Ecology 51:565–581.Google Scholar
  26. Feeny, P. 1975. Biochemical coevolution between plants and their insect herbivores, pp. 3–19,in L.E. Gilbert and P.H. Raven (eds.). Coevolution of Animals and Plants. University of Texas Press, Austin.Google Scholar
  27. Haupt, I. 1976. Separation of the sites of synthesis and accumulation of 3,4-dihydroxyphenyl-alanine inEuphorbia lathyris L.Nova Acta Leopold. Suppl. 7:129–132.Google Scholar
  28. Isman, M.B., Duffey, S.S., andScudder, G.G.E. 1977a. Cardenolide content of some leaf-and stem-feeding insects on temperate North American milkweeds (Asclepias spp.).Can J. Zool. 55:1024–1028.Google Scholar
  29. Isman, M.B., Duffey, S.S., andScudder, G.G.E. 1977b. Variation in cardenolide content of the Lygaeid Bugs,Oncopeltus fasciatus andLygaeus kalmii kalmii and of their milkweed hosts (Asclepias spp.) in central California.J. Chem. Ecol. 3:613–624.Google Scholar
  30. Jones, D.A. 1972. Cyanogenic glycosides and their function, pp. 103–124,in J.B. Harborne (ed.). Phytochemical Ecology. Academic Press, New York.Google Scholar
  31. Jungreis, A.M., andVaughan, G.L. 1977. Insensitivity of lepidopteran tissues to ouabain: Absence of ouabain binding and Na+-K+ ATPases in larval and adult midgut.J. Insect Physiol. 23:503–509.Google Scholar
  32. Karawya, M.S., Balbaa, S.I., andKhayyal, S.E. 1973. Estimation of Cardenolides inNerium oleander.Planta Med. 23:70–73.PubMedGoogle Scholar
  33. Kingsbury, J.M. 1964. Poisonous Plants of the United States and Canada. Prentice-Hall, New Jersey.Google Scholar
  34. Kojima, M., Poulton, J.E., Thayer, S.S., andConn, E.E. 1979. Tissue distributions of dhurrin and of enzymes involved in its metabolism in leaves ofSorghum bicolor.Plant Physiol. 63:1022–1028.Google Scholar
  35. Kupchan, S.M., Mokotoff, M., Sandhu, R.S., andHokin, L.E. 1967. The chemistry and biological activity of derivatives of strophanthidin.J. Med. Chem. 10:1025–1033.PubMedGoogle Scholar
  36. Kupchan, S.M., Uchida, I., Shimada, K., Yu Fri, B., Stevens, D.M., Sneden, A.T., Miller, R.W., andBryan, R.F. 1977. Elaeodendroside A: a novel cytotoxic cardiac glycoside fromElaeodendron glaucum.J. Chem. Soc. Chem. Commun. 1977:255–256.Google Scholar
  37. Levin, D.A. 1971. Plant phenolics: An ecological perspective.Am. Nat. 105:157–181.Google Scholar
  38. Levin, D.A. 1976. The chemical defenses of plants to pathogens and herbivores.Annu. Rev. Ecol. Syst. 7:121–159.Google Scholar
  39. Loffelhardt, W., Kopp, B., andKubelka, W. 1979. Intracellular distribution of cardiac glycosides in leaves ofConvallaria majalis.Phytochemistry 18:1289–1291.Google Scholar
  40. MacRobbie, E.A.C. 1962. Ionic relatons ofNitella translucens.J. Gen. Physiol. 45:861–878.Google Scholar
  41. Masler, L., Bauer, Ŝ., Bauerová, O. andŜikl, D. 1962. Cardiac glycosides ofAsclepias syriaca L. I. Isolation of the cardio-active steroids.Collect. Czech. Chem. Commun. 27:872–881.Google Scholar
  42. Matile, P. 1976. Localization of alkaloids and mechanism of their accumulation in vacuoles ofChelidonium majus laticifers.Nova Acta Leopold. Suppl. 7:139–156.Google Scholar
  43. Matile, P., Jans, B., andRickenbacher, R. 1970. Vacuoles ofChelidonium latex: Lysosomal property and accumulation of alkaloids.Biochem. Physiol. Pflanzen 161:447–458.Google Scholar
  44. McKey, D. 1974. Adaptive patterns in alkaloid physiology.Am. Nat. 108:305–320.Google Scholar
  45. McKey, D. 1979. The distribution of secondary compounds within plants, pp. 55–133,in G.A. Rosenthal and D.H. Janzen (eds.). Herbivores. Academic Press, New York.Google Scholar
  46. Mülles, E. 1976. Principles in transport and accumulation of secondary products.Nova Acta Leopold. Suppl. 7:123–128.Google Scholar
  47. Neumann, D. 1976. Interrelationship between the morphology of alkaloid storage cells and the possible mechanism of alkaloid storage.Nova Acta Leopold. Suppl. 7:77–81.Google Scholar
  48. Nie, N.H., Hull, C.H., Jenkins, J.G., Steinbrenner, K., andBent, D.U. 1977. Statistical Package for the Social Sciences, SPSS 6000, 2nd ed., Version 7. McGraw-Hill, New York.Google Scholar
  49. Pasteels, J.M., Daloze, D., van Dorsser, W., andRoba, J. 1979. Cardiac glycosides in the defensive secretion ofChrysolina herbacea (Coleoptera, Chrysomelidae). Identification, biological role and pharmacological activity.Comp. Biochem. Physiol. 63C:117–121.Google Scholar
  50. Price, P.W., andWillson, M.F. 1979. Abundance of herbivores on six milkweed species in Illinois.Am. Midl. Nat. 101:76–86.Google Scholar
  51. Rafaeli-Bernstein, A., andMordue, W. 1978. The transport of the cardiac glycoside ouabain by the Malpighian tubules ofZonocerus variegatus.Physiol. Entomol. 3:59–63.Google Scholar
  52. Rhoades, D.F., andCates, R.G. 1976. A general theory of plant antiherbivore chemistry, pp. 168–213,in J.W. Wallace and R.L. Mansell (eds.). Recent Advances in Phytochemistry, Biochemical Interactions between Plants and Insects, Vol. 10. Plenum Press, New York.Google Scholar
  53. Roeske, C.N., Seiber, J.N., Brower, L.P., andMoffitt, C.M. 1976. Milkweed cardenolides and their comparative processing by monarch butterflies (Danaus plexippus L.), pp. 93–167,in J.W. Wallace and R.L. Mansell (eds.). Recent Advances in Phytochemistry, Biochemical Interactions between Plants and Insects, Vol. 10. Plenum Press, New York.Google Scholar
  54. Rothschild, M., andReichstein, T. 1976. Some problems associated with the storage of cardiac glycosides by insects.Nova Acta Leopold. Suppl. 7:507–550.Google Scholar
  55. Rowson, J.M. 1952. Studies in the genusDigitalis, Part I. The colorimetric estimation of digitoxin and preparations ofDigitalis purpurea.J. Pharm. Pharmacol. 4:814–830.PubMedGoogle Scholar
  56. Scriber, J.M. 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. 24:494–510.Google Scholar
  57. Seiber, J.N.,Nelson, J.C., andLee, S.M. 1981. Cardenolides in the latex and leaves of sevenAsclepias species andCalotropis procera. Submitted for publication.Google Scholar
  58. Seiber, J.N., Roeske, C.N., andBenson, J.M. 1978. Three new cardenolides from the milkweedsAsclepias eriocarpa andA. labriformis.Phytochem. 17:967–970.Google Scholar
  59. Seiber, J.N., Tuskes, P.M., Brower, L.P., andNelson, C.J. 1980. Pharmacodynamics of some individual milkweed cardenolides fed to larvae of the monarch butterfly.J. Chem. Ecol. 6:321–339.Google Scholar
  60. Seigler, D.S. 1977. Primary roles for secondary compounds.Biochem. Syst. Ecol. 5:195–199.Google Scholar
  61. Swain, T. 1976. Secondary compounds: Primary products.Nova Acta Leopold. Suppl. 7:411–421.Google Scholar
  62. Swain, T. 1977. Secondary compounds as protective agents.Annu. Rev. Plant Physiol. 28:479–501.Google Scholar
  63. Thomashow, P. 1975. The paradox of the cryptic chrysalid. Senior honors thesis, Amherst College, Amherst, Massachusetts.Google Scholar
  64. Vaughan, F.A. 1979. Effect of gross cardiac glycosides of seeds of common milkweed,Asclepias syriaca, on cardiac glycoside uptake by the milkweed bugOncopeltus fasciatus.J. Chem. Ecol. 5:89–100.Google Scholar
  65. Vaughan, G.L., andJungreis, A.M. 1977. Insensitivity of Lepidopteran tissues to ouabain: Physiological mechanisms for protection from cardiac glycosides.J. Insect Physiol. 23:585–589.Google Scholar

Copyright information

© Plenum Publishing Corporation 1981

Authors and Affiliations

  • C. J. Nelson
    • 1
  • J. N. Seiber
    • 1
  • L. P. Brower
    • 2
  1. 1.Department of Environmental ToxicologyUniversity of CaliforniaDavis
  2. 2.Department of ZoologyUniversity of FloridaGainesville

Personalised recommendations