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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

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Abstract

This paper is the first in a series on cardenolide fingerprinting of the monarch butterfly. New methodologies are presented which allow both qualitative and quantitative descriptions of the constituent cardenolides which these insects derive in the wild from specificAsclepias foodplants. Analyses of thin-layer Chromatographic profiles ofAsclepias eriocarpa cardenolides in 85 individual plant-butterfly pairs collected at six widely separate localities in California indicate a relatively invariant pattern of 16–20 distinct cardenolides which we here define as theAsclepias eriocarpa cardenolide fingerprint profile. Cardenolide concentrations vary widely in the plant samples, but monarchs appear able to regulate total storage by increasing their concentrations relative to their larval host plant when reared on plants containing low concentrations, and vice versa. Forced-feeding of blue jays with powdered butterfly and plant material and with one of the constituent plant cardenolides, labriformin, established that theA. eriocarpa cardenolides are extremely emetic, and that monarchs which have fed on this plant contain an average of 16 emetic-dose fifty (ED50) units. The relatively nonpolar labriformin and labriformidin in the plant are not stored by the monarch but are metabolized in vivo to desglucosyrioside which the butterfly does store. This is chemically analogous to the way in which monarchs and grasshoppers metabolize another series of milkweed cardenolides, those found inA. curassavica. It appears that the sugar moiety through functionality at C-3′ determines which cardenolides are metabolized and which are stored. The monarch also appears able to store several lowR f cardenolides fromA. eriocarpa without altering them. Differences in the sequestering process in monarchs and milkweed bugs (Oncopeltus) may be less than emphasized in the literature. The monarch is seen as a central organism involved in a coevolutionary triad simultaneously affecting and affected by both its avian predators and the secondary chemistry of the milkweeds with which it is intimately involved.

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References

  • Abisch, E., andReichstein, T. 1962. Orientierende chemische Untersuchung einiger Asclepiadaceen und Periplocaceen.Helv. Chim. Acta 45:2090–2116.

    Google Scholar 

  • Agnew, A.D.Q. 1974. Upland Kenya Wildflowers. Oxford University Press, Oxford, x + 827 pp.

    Google Scholar 

  • Atsatt, P., andO'dowd, D.J. 1976. Plant defense guilds.Science 193:24–29.

    Google Scholar 

  • Baker, H.G., andBaker, I. 1975. Studies of nectar constitution and pollination-plant coevolution, pp. 100–140,in L.E. Gilbert and P.H. Raven (eds.). Coevolution of Animals and Plants, University of Texas Press, Austin.

    Google Scholar 

  • Barbosa, P., andGreenblatt, J. 1979. Effects of leaf age and position on larval preference of the fall webworm,Hyphantria cunea (Lepid. Arctiidae).Can. Entomol 111:381–383.

    Google Scholar 

  • Barney, W. P., andRock, G.C. 1975. Consumption and utilization by the Mexican bean beetle of soybean plants varying in levels of resistance.J. Econ. Entomol. 68:497–501.

    Google Scholar 

  • Barthakur, P. 1971. Wang Laboratory 700 Series Program Library 9. Wang Laboratories, Tewksbury, Massachusetts.

    Google Scholar 

  • Benson, J.M., andSeiber, J.N. 1978. High-speed liquid chromatography of cardiac glycosides in milkweed plants and monarch butterflies.J. Chromatogr. 148:521–527.

    Google Scholar 

  • Benson, J.M., Seiber, J.N., Keller, R.F., andJohnson, A.E. 1978. Studies on the toxic principle ofAsclepias eriocarpa andAsclepias labriformis, pp. 273–284,in R.F. Keller, K.R. van Kampen, and L. F. James (eds.). Effects of Poisonous Plants on Livestock. Academic Press, New York.

    Google Scholar 

  • 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.

    Google Scholar 

  • Boppré, M. 1978. Chemical communication, plant relationships, and mimicry in the evolution of danaid butterflies.Entomol Exp. Appl. 24:264–277.

    Google Scholar 

  • 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 

  • Botha, C.E.J., Malcolm, S.B., andEvert, R.F. 1977. An investigation of preferential feeding habits in four Asclepiadaceae by the aphidAphis nerii.Protoplasma 92:1–20.

    Google Scholar 

  • Boyd, C.E., andGoodyear, C.P. 1971. Nutritive quality of food in ecological systems.Arch. Hydrobiol. 69:256–270.

    Google Scholar 

  • Bowers, M.D. 1980. Unpalatability as a defense strategy ofEuphydryas phaeton (Lepidoptera: Nymphaudae).Evolution 34:586–600.

    Google Scholar 

  • Brattsten, L.B., Wilkinson, C.F., andEisner, T. 1977. Herbivore-plant interactions: Mixed-function oxidases and secondary plant substances.Science 196:1349–1352.

    Google Scholar 

  • Brewer, J. Short-lived phenomena.News Lepid. Soc. 1977(4): 7.

  • Brower, L.P. 1970. Plant poisons in a terrestrial food chain and implications for mimicry theory, pp. 69–82,in K.L. Chambers (ed.). Biochemical Coevolution. Proc. 29th Annual Biology Colloquium. Oregon State University, Corvallis, Oregon.

    Google Scholar 

  • Brower, L.P. 1977. Monarch migration.Nat. Hist. 86(June–July):40–53.

    Google Scholar 

  • Brower, L.P., andBrower, J.V.Z. 1964. Birds, butterflies, and plant poisons: A study in ecological chemistry.Zoologica 49:137–159.

    Google Scholar 

  • Brower, L.P., andGlazier, S.C. 1975. Localization of heart poisons in the monarch butterfly.Science 188:19–25.

    Google Scholar 

  • Brower, L.P., andMoffitt, C.M. 1974. Palatability dynamics of cardenolides in the monarch butterfly.Nature 249:280–283.

    Google Scholar 

  • Brower, L.P., Brower, J.V.Z., andCorvino, J.M. 1967. Plant poisons in a terrestrial foodchain.Proc. Natl. Acad. Sci. U.S.A. 57:893–898.

    Google Scholar 

  • Brower, L.P., Ryerson, W.N., Coppinger, L.L., andGlazier, S.C. 1968. Ecological chemistry and the palatability spectrum.Science 161:1349–1351.

    Google Scholar 

  • Brower, L.P., McEvoy, P.B., Williamson, K.L., andFlannery, M.A. 1972. A new cardiac giycoside assay and the palatability spectrum in natural populations of monarch butterflies.Science 177:426–429.

    Google Scholar 

  • 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 

  • Brower, L.P., Calvert, W.H., Hedrick, L.E., andChristian, J. 1977. Biological observations on an overwintering colony of monarch butterflies (Danaus plexippus, Danaidae) in Mexico.J. Lepid. Soc. 31:232–242.

    Google Scholar 

  • Brower, L.P., Gibson, D.O., Moffitt, C.M., andPanchen, A.L. 1978. Cardenolide content ofDanaus chrysippus butterflies from three regions of East Africa.Biol. J. Linn. Soc. 10:251–273.

    Google Scholar 

  • Brower, L.P.,Calvert, W.H.,Glazier, S.C., andSheppard, M. 1982a. The cardenolide content of overwintering monarch butterflies in Mexico. In preparation.

  • Brower, L.P.,Calvert, W.H., andWalford, P. 1982b. Nectar starvation and lipid utilization in overwintering monarch butterflies in Mexico. In preparation.

  • Brower, L.P.,Fink, —., andWaide, —. 1982c. In preparation.

  • Brown, P., Von Euw, J., v.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 

  • Brüschweiler, F., Stöckel, K., andReichstein, T. 1969.Calotropis—Glykoside, vermutliche Teilstruktur.Helv. Chim. Acta 52:2276–2303.

    Google Scholar 

  • Calvert, W.H., Hedrick, L.E., andBrower, L.P. 1979. Mortality of the monarch butterfly (Danaus plexippus L.): Avian predation at five overwintering sites in Mexico.Science 204:847–851.

    Google Scholar 

  • Cates, R.G., andOrians, G.H. 1975. Successional status and the palatability of plants to generalized herbivores.Ecology 56:410–418.

    Google Scholar 

  • 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 

  • Chaney, S.G., andKare, M.R. 1966. Emesis in birds.J. Am. Vet. Med. Assoc. 149:938–943.

    Google Scholar 

  • Cheung, H.T., Watson, T.R., Seiber, J.N., andNelson, C.J. 1980. 7β, 8β-Epoxycardenolide glycosides ofAsclepias eriocarpa.J. Chem. Soc. Perkin Trans. I 1980:2169–2173.

    Google Scholar 

  • Chew, F.S., andRodman, J.E. 1979. Plant resources for chemical defense, pp. 271–307,in G.A. Rosenthal and D.H. Janzen (eds.). Herbivores, Their Interactions with Secondary Plant Metabolites. Academic Press, New York.

    Google Scholar 

  • Cooper-Driver, G.A., andSwain, T. 1976. Cyanogenic polymorphism in bracken in relation to herbivore predation.Nature 260:604.

    Google Scholar 

  • Coulman, B.E., Clark, K.W., andWoods, D.L. 1977a. Effects of selected reed canary grass alkaloids on in vitro digestibility.Can. J. Plant Sci. 57:779–785.

    Google Scholar 

  • Coulman, B.E., Woods, D.L., andClark, K.W. 1977b. Distribution within the plant, variation with maturity, and heritability of gramine and hordenine in reed canary grass.Can. J. Plant Sci. 57:771–777.

    Google Scholar 

  • Dadd, R.H. 1973. Insect nutrition: Current developments and metabolic implications.Annu. Rev. Entomol. 18:381–420.

    Google Scholar 

  • Dean, R.B., andDixon, W. J. 1951. Simplified statistics for small numbers of observations.Anal. Chem. 23:636–638.

    Google Scholar 

  • Dewaal, D. 1942. Het Cyanophore Kakakter van witte Klauver,Trifolium repens L. Thesis, H. Veenmanen Zonen N.V., Wageningen, Netherlands.

  • Dingle, H. 1978. Migration and diapause in tropical, temperate, and island milkweed bugs, pp. 254–276,in H. Dingle (ed.). Evolution of Insect Migration and Diapause. Springer-Verlag, New York.

    Google Scholar 

  • Dixon, C.A., Erickson, J.M., Kellett, D.N., andRothschild, M. 1978. Some adaptations betweenDanaus plexippus and its foodplant, with notes onDanaus chrysippus andEuploea core (Insecta: Lepidoptera).J. Zool. London 185:437–467.

    Google Scholar 

  • Dixon, W. J., andMassey, F. J. 1957. Introduction to Statistical Analysis, 2nd. ed. McGraw-Hill Book Co., Inc., New York.

    Google Scholar 

  • Dolinger, P.M., Ehrlich, P.R., Fitch, W.L., andBreedlove, D.E. 1973. Alkaloid and predation patterns in Colorado lupine populations.Oecologia (Berlin) 13:191–204.

    Google Scholar 

  • Duffey, S.S. 1977. Arthropod allomones: Chemical effronteries and antagonists.XVth. Int. Congr. Entomol., 1976. Washington, D.C. pp. 323–394.

  • Duffey, S.S. 1980. Sequestration of plant natural products by insects.Annu. Rev. Entomol 25:447–477.

    Google Scholar 

  • Duffey, S.S., andScudder, G.G.E. 1972. Cardiac glycosides in North American Asclepiadaceae, a basis for unpalatability in brightly coloured Hemiptera and Coleoptera.J. Insect Physiol. 18:63–78.

    Google Scholar 

  • Duffey, S.S., andScudder, G.G.E. 1974. Cardiac glycosides inOncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae). I. The uptake and distribution of natural cardenolides in the body.Can. J. Zool. 52:283–290.

    Google Scholar 

  • 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 

  • Edgar, J.A., Culvenor, C.C.J., andPliske, T.E. 1974. Co-evolution of danaid butterflies with their host plants.Nature 250:646–648.

    Google Scholar 

  • Edgar, J.A., Cockrum, P.A., andFrahan, J.L. 1976. Pyrrolizidine alkaloids inDanaus plexippus L. andDanaus chrysippus L.Experentia 32:1535–1537.

    Google Scholar 

  • Edgar, J.A., Boppré, M., andSchneider, D. 1979. Pyrrolizidine alkaloid storage in African and Australian danaid butterflies.Experientia 35:1447–1448.

    Google Scholar 

  • Ehrlich, P.R. 1970. Coevolution and the biology of communities, pp. 1–11,in K.L. Chambers (ed.). Biochemical Coevolution. Oregon State University Press, Corvallis, Oregon.

    Google Scholar 

  • Ehrlich, P.R., andRaven, P.H. 1965. Butterflies and plants: A study in Coevolution.Evolution 18:586–608.

    Google Scholar 

  • Ellis, W.M., Keymer, R.J., andJones, D.A. 1977a. On the polymorphism of cyanogenesis inLotus corniculatus L. VIII. Ecological studies in Anglesey.Heredity 39:45–65.

    Google Scholar 

  • Ellis, W.M., Keymer, R.J., andJones, D.A. 1977b. The effect of temperature on the polymorphism of cyanogenesis inLotus corniculatus L.Heredity 38:339–347.

    Google Scholar 

  • Evans, F.J., andCowley, P.S. 1972. Cardenolides and spirostanols inDigitalis purpurea at various stages of development.Phytochemistry 11:2971–2975.

    Google Scholar 

  • 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 

  • Feeny, P. 1975. Biochemical Coevolution between plants and their insect herbivores, pp. 3–19,in L.E. Gilbert and P.M. Raven(eds.). Coevolution of Animals and Plants. University of Texas Press, Austin, Texas.

    Google Scholar 

  • Feeny, P. 1976. Plant apparency and chemical defense.Rec. Adv. in Phytochem. 10:1–40.

    Google Scholar 

  • Feeny, P. 1977. Defensive ecology of the Cruciferae.Ann. Mo. Bot. Garden 64:221–234.

    Google Scholar 

  • Feir, D., andSuen, J. 1971. Cardenolides in the milkweed plant and feeding by the milkweed bug.Ann. Entomol. Soc. Am. 64:1173–1174.

    Google Scholar 

  • Ferm, R. 1977. A comparative study of cardiac glycoside sequestering byDanaus plexippus andDanaus chrysippus. Honors thesis, Amherst College.

  • Fink, L.S., andBrower, L.P. 1981. Birds can overcome the cardenolide defence of monarch butterflies in Mexico.Nature 291:67–70.

    Google Scholar 

  • Fox, L.R., andMacauley, B.J. 1977. Insect grazing onEucalyptus in response to variation in leaf tannins and nitrogen.Oecologia (Berlin) 29:145–162.

    Google Scholar 

  • Fraenkel, G.S. 1959. The raison d'etre of secondary plant substances.Science 129:1466–1470.

    Google Scholar 

  • Futuyma, D. J. 1976. Foodplant specialization and environmental predictability in Lepidoptera.Am. Nat. 110:285–292.

    Google Scholar 

  • Garcia, J. 1980. Tilting at the papermills of academe. American Psychological Association, 1980 address, Montreal, Canada, pp. 1–31.

    Google Scholar 

  • Garcia, J., andHankins, W.G. 1975. Evolution of bitter and the acquisition of toxophobia, pp. 39–45,in D.A. Denton and J.P. Coghlan (eds.). Olfaction and Taste, Vol. 5. Academic Press, New York.

    Google Scholar 

  • Gilbert, L.E., andRaven, P.M. 1975. General introduction, pp. ix-xiii,in L.E. Gilbert and P.H. Raven (eds.). Coevolution of Animals and Plants. University of Texas Press, Austin, Texas.

    Google Scholar 

  • Harborne, J.B. 1977. Introduction to Ecological Biochemistry. Academic Press, New York.

    Google Scholar 

  • Heinrich, B. 1979. Bumblebee Economics. Harvard University Press, Cambridge, Massachusetts.

    Google Scholar 

  • Hesse, G., andLudwig, G. 1960. Voruscharin, ein zweites schwefelhaltiges Herzgift ausCalotropis procera L.Liebigs Ann. Chem. 632:158–171.

    Google Scholar 

  • Hirotani, M., andFuruya, T. 1977. Restoration of cardenolide synthesis in redifferentiated shoots from callus cultures ofDigitalispurpurea.Phytochemistry 16:610–611.

    Google Scholar 

  • House, H.L. 1969. Effects of different proportions of nutrients on insects.Entomol. Exp. Appl. 12:659–669.

    Google Scholar 

  • Isman, M.B. 1977. Dietary influence of cardenolides on larval growth and development of the milkweed bugOncopeltus fasciatus.J. Insect Physiol. 23:1183–1187.

    Google Scholar 

  • Isman, M.B., Duffey, S.S., andScudder, G.G.E. 1977a. 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 

  • Isman, M.B., Duffey, S.S., andScudder, G.G.E. 1977b. Cardenolide content of some leaf-and stem-feeding insects on temperate North American milkweeds (Asclepias spp.).Can. J. Zool. 55:1024–1028.

    Google Scholar 

  • Janzen, D.H. 1980. When is it coevolution?Evolution 34:611–612.

    Google Scholar 

  • Jones, D.A. 1973. Co-evolution and cyanogenesis, pp. 213–242,in V.H. Heywood (ed.). Taxonomy and Ecology. Academic Press, New York.

    Google Scholar 

  • Jones, D.A., Keymer, R.J., andEllis, W.M. 1978. Cyanogenesis in plants and animal feeding, pp. 21–34,in J.B. Harborne (ed.). Biochemical Aspects of Plant and Animal Coevolution. Academic Press, New York.

    Google Scholar 

  • Karawya, M.S., Balboa, S.I., andKhayyal, S.E. 1973. Estimation of cardenolides inNerium oleander.Planta Med. 23:70–73.

    Google Scholar 

  • Koeppe, D.K., Southwick, L.M., andBittell, J.E. 1976. The relationship of tissue chlorogenic acid concentrations and leaching of phenolics from sunflowers grown under varying phosphate nutrient conditions.Can. J. Bot. 54:593–599.

    Google Scholar 

  • Kuchokhidze, D.K., Puchkova, E.I., Kolomhtseva, T.N., andEristavi, L.I. 1974. Dynamics of the accumulation of cardiac glycosides in the leaves ofRhodeajaponica depending on the conditions of growth and the phase of development.Tbilis Gos. Med. Inst. Tbilisi(U.S.S.R.) 74:621–624.

    Google Scholar 

  • Laycock, W.A. 1975. Alkaloid content of duncecap larkspur after two years of clipping.J. Range Manage. 28:257–259.

    Google Scholar 

  • Laycock, W.A. 1978. Coevolution of poisonous plants and large herbivores on rangelands.J. Range Manage. 31:335–342.

    Google Scholar 

  • Levin, D.A. 1976a. Alkaloid-bearing plants: An ecogeographic perspective.Am. Nat 110: 261–284.

    Google Scholar 

  • Levin, D.A. 1976b. The chemical defenses of plants to pathogens and herbivores.Annu. Rev. Ecol. Syst. 7:121–159.

    Google Scholar 

  • Levin, D.A., andYork, B.M., Jr. 1978. The toxicity of plant alkaloids: An ecogeographic perspective.Kochern. Syst. Ecol. 6:61–76.

    Google Scholar 

  • Marsh, N.A., Clarke, C.A., Rothschild, M., andKellett, D.N. 1977.Hypolimnas bolina (L.), a mimic of danaid butterflies, and its modelEuploea core (Cram.) store cardioactive substances.Nature 268:726–728.

    Google Scholar 

  • Masler, L., Bauer, S., BauerovÁ, O., andSikl, D. 1961. Herzglykoside der Scidenpflanze (Asclepias syriaca L.) I. Isolierung der Herzwirksamen steroide.Experientia 17:872–881.

    Google Scholar 

  • Mathavan, S., andBhaskaran, R. 1975. Food selection and utilization in a danaid butterfly.Oecologia (Berlin) 18:55–62.

    Google Scholar 

  • Mathavan, S., andPandian, T. J. 1975. Effect of temperature on food utilization in the monarch butterflyDanaus chrysippus.Oikos 26:60–64.

    Google Scholar 

  • Mathavan, S., Pandian, T.J., andMary, M.J. 1976. Use of feeding rate as an indicator of caloric value in some Lepidopterous larvae.Oecologia (Berlin) 24:91–94.

    Google Scholar 

  • McKey, D. 1979. The distribution of secondary compounds within plants, pp. 55–133,in G.A. Rosenthal and D.H. Janzen (eds.). Herbivores, Their Interaction with Secondary Plant Metabolites. Academic Press, New York.

    Google Scholar 

  • McKey, D., Waterman, P.G., Mbi, C.N., Gartlan, J.S., andStruhsaker, T.T. 1978. Phenolic content of vegetation of two African rain forests: Ecological implications.Science 202:61–64.

    Google Scholar 

  • Mothes, K. 1976. Secondary plant substances as materials for chemical high quality breeding in higher plants.Rec. Adv. Phytochem. 10:385–405.

    Google Scholar 

  • Neher, R. 1969. TLC of steroids and related compounds, p. 311, in E. Stahl (ed.). Thin-Layer Chromatography, A Laboratory Handbook. Springer-Verlag, New York.

    Google Scholar 

  • Nelson, C.J., Seiber, J.N., andBrower, L.P. 1981. Seasonal and intraplant variation of cardenolide content in the California milkweed,Asclepias eriocarpa, and implications for plant defense.J. Chem. Ecol. 7:981–1010.

    Google Scholar 

  • Pandian, T.J., Pitchairaj, R., Mathavan, S., andPalanichamy, R. 1978. Effects of temperature and leaf ration on the water budget of the final instar larvae ofDanaus chrysippus L. (Lepidoptera: Danaidae).Monitore Zool. Ital. (N.S.) 12:17–28.

    Google Scholar 

  • Parker, R., andWilliams, M.C. 1974. Factors affecting miserotoxin metabolism in Timber Milkvetch.Weed Sci. 22:552–556.

    Google Scholar 

  • Parsons, J.A. 1965. A digitalis-like toxin in the monarch butterfly,Danaus plexippus L.J. Physiol. 178:290–304.

    Google Scholar 

  • Price, P.W., andWillson, M.F. 1979. Abundance of herbivores on six milkweed species in Illinois.Am. Midl. Nat. 101:76–86.

    Google Scholar 

  • Price, P.W., Boulton, C.E., Gross, P., McPheron, B.A., Thompson, J.N., andWeis, A.E. 1980. Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies.Annu. Rev. Ecol. Syst. 11:41–65.

    Google Scholar 

  • Rafaeli-Bernstein, A., andMordue, W. 1978. The transport of the cardiac glycoside ouabain by the malphigian tubules ofZonocerus variegatus.Physiol. Entomol. 3:59–63.

    Google Scholar 

  • Reichstein, T., Von Euw, J., Parsons, J.A., andRothschild, M. 1968. Heart poisons in the monarch butterfly.Science 161:861–866.

    Google Scholar 

  • Rhoades, D.F., andCates, R.G. 1976. Toward a general theory of plant antiherbivore chemistry.Rec. Adv. Phytochem. 10:168–213.

    Google Scholar 

  • Rodman, J.E., andChew, F.S. 1980. Phytochemical correlates of herbivory in a community of native and naturalized Cruciferae.Biochem. Ecol. Syst. 8:43–50.

    Google Scholar 

  • Roeske, C.N., Seiber, J.S., Brower, L.P., andMoffitt, C.M. 1976. Milkweed cardenolides and their comparative processing by monarch butterflies (Danaus plexippus L.).Rec. Adv. Phytochem. 10:93–167.

    Google Scholar 

  • Rosenthal, G. A., andJanzen, D.H. (eds.). 1979. Herbivores, Their Interaction with Secondary Plant Metabolites. Academic Press, New York, xvi + 718 pp.

    Google Scholar 

  • Rothschild, M. 1973. Secondary plant substances and warning coloration in insects, pp. 59–83,in H.F. van Emden (ed.). Insect/Plant Relationships. Symposium of the Royal Entomological Society, London, Vol. 6.

  • Rothschild, M. 1977. The cat-like caterpillar.News Lepid. Soc. 1977(6):9.

    Google Scholar 

  • Rothschild, M., andEdgar, J.A. 1978. Pyrrolizidine alkaloids fromSenecio vulgaris sequestered and stored byDanaus plexippus. J. Zool. London 186:347–349.

    Google Scholar 

  • Rothschild, M., andFord, B. 1970. Heart poisons and the monarch.Nat. Hist. 79(4): 36–37.

    Google Scholar 

  • Rothschild, M., andKellett, D.N. 1972. Reactions of various predators to insects storing heart poisons (cardiac glycosides) in their tissues.J. Entomol. (A) 46:103–110.

    Google Scholar 

  • Rothschild, M., andMarsh, N. 1978. Some peculiar aspects of Danaid/plant relationships.Entomol. Exp. Appl. 24:437–450.

    Google Scholar 

  • Rothschild, M., Reichstein, T., andVon Euw, J. 1973. (no title).Proc. R. Entomol. Soc. London 37(9): 37–38.

    Google Scholar 

  • Rothschild, M., von Euw, J., Reichstein, T., Smith, D.A.S., andPierre, J. 1975. Cardenolide storage inDanaus chrysippus (L.) with additional notes onD. plexippus.Proc. R. Soc. London, Ser. B 190:1–31.

    Google Scholar 

  • 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.

    Google Scholar 

  • Schroeder, L.A. 1976. Energy, matter and nitrogen utilization by the larvae of the monarch butterflyDanaus plexippus.Oikos 27:259–264.

    Google Scholar 

  • Schweitzer, D.F. 1979. Effects of foliage age on body weight and survival in larvae of the tribe Lithophanini (Lepidoptera: Noctuidae).Oikos 32:403–408.

    Google Scholar 

  • Scriber, J.M. 1977. Limiting effects of low leaf-water content on the nitrogen utilization, energy budget, and larval growth ofHyalophora cecropia (Lepidoptera: Saturniidae).Oecologia (Berlin) 28:269–287.

    Google Scholar 

  • Scriber, J.M., andSlansky, F., Jr. 1981. The nutritional ecology of immature insects.Annu. Rev. Entomol. 26:183–211.

    Google Scholar 

  • Seiber, J.N., Roeske, C.N., andBenson, J.M. 1978. Three new cardenolides from the milkweedsAsclepias eriocarpa andA. labriformis.Phytochemistry 17:967–970.

    Google Scholar 

  • Seiber, J.N., Tuskes, P.M., Brower, L.P., andNelson, C.J. 1980. Pharmacodynamics of some individual cardenolides fed to larvae of the monarch butterfly (Danaus plexippus L.).J. Chem. Ecol. 6:321–339.

    Google Scholar 

  • Sinden, S.L., Schalk, J.M., andStoner, A.K. 1978. Effects of daylength and maturity of tomato plants on tomatine content and resistance to the Colorado potato beetle.J. Am. Soc. Hortic. Sci. 103:596–600.

    Google Scholar 

  • Slansky, F., Jr., andFeeny, P. 1977. Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on the wild and cultivated foodplants.Ecol. Monogr. 47:209–228.

    Google Scholar 

  • Steel, R.G.D., andTorrie, J.H. 1960. Principles and Procedures in Statistics. McGraw-Hill Book Co., New York, 481 pp.

    Google Scholar 

  • Stoll, A. 1940. The Cardiac Glycosides. The Pharmaceutical Press, London.

    Google Scholar 

  • Sturgeon, K.B. 1979. Monoterpene variation in ponderosa pine xylem related to western pine beetle predation.Evolution 33:803–814.

    Google Scholar 

  • Swain, T. 1977. Secondary compounds as protective agents.Annu. Rev. Plant Physiol. 28:479–501.

    Google Scholar 

  • Tahsler, B.D. 1975. The distribution of cardenolides inAsclepias curassavica andA. nivea and its effect on the uptake of cardenolides by monarch butterfly larvae: Implications for the cardenolide dynamics of natural monarch populations. Honors thesis, Amherst College, Amherst, Massachusetts.

    Google Scholar 

  • Taylor, W.I. 1963. Alkaloids, pp. 758–778,in A. Standen (ed.). Kirk-Othmer Encyclopedia of Chemical Technology, 2nd. ed., Vol. 1. Interscience, New York.

    Google Scholar 

  • Thomashow, P. 1975. The paradox of the cryptic chrysalid. Honors thesis, Hampshire College, Amherst, Massachusetts.

    Google Scholar 

  • Tuskes, P.M., andBrower, L.P. 1978. Overwintering ecology of the monarch butterfly,Danaus plexippus L., in California.Ecol. Entomol. 3:141–153.

    Google Scholar 

  • Urquhart, F.A. 1960. The Monarch Butterfly. University of Toronto Press, Toronto, Canada, xxiv + 361 pp.

    Google Scholar 

  • Urquhart, F. A., andUrquhart, N.R. 1976. The overwintering site of the eastern population of the monarch butterfly (Danaus plexippus; Danaidae) in southern Mexico.J. Lepid. Soc. 30:153–158.

    Google Scholar 

  • Urquhart, F.A. andUrquhart, N.R. 1979. Vernal migration of the monarch butterfly (Danaus p. plexippus, Lepidoptera: Danaidae) in North America from the overwintering site in the neo-volcanic plateau of Mexico.Can. Entomol. 111:15–18.

    Google Scholar 

  • Vaughan, F.A.1979. Effect of gross cardiac glycoside content of seeds of common milkweedAsclepias syriaca, on cardiac glycoside uptake by the milkweed bugOncopeltus fasciatus.J. Chem. Ecol. 5:89–100.

    Google Scholar 

  • 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 

  • Von Euw, J., Fishelson, L., Parsons, J.A., Reichstein, T. andRothschild, M. 1967. Cardenolides (heart poisons) in a grasshopper feeding on milkweeds.Nature 214:35–39.

    Google Scholar 

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

    Google Scholar 

  • Whittaker, R.H. andFeeny, P.1971. Allelochemics: Chemical interactions between species.Science 171:757–770.

    Google Scholar 

  • Wichtl, M.V. 1975. Chemische Rassen bei Glykosidpflanzen.Planta Med. 28:257–268.

    Google Scholar 

  • Woodson, R.E., Jr.1954. The North American species ofAsclepias L.Ann. Mo. Bot. Garden 41:1–211.

    Google Scholar 

  • Yoder, C.A., Leonard, D.E. andLerner, J. 1976. Intestinal uptake of ouabain and digitoxin in the milkweed bug,Oncopeltus fasciatus.Experientia 32:1549–1550.

    Google Scholar 

  • Zar, J.H. 1974. Biostatistical Analysis. Prentice Hall, Englewood Cliffs, New Jersey, xvi + 620 pp.

    Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, University of Florida, 32611, Gainesville, Florida

    L. P. Brower

  2. Department of Environmental Toxicology, University of California, 95616, Davis, California

    J. N. Seiber, C. J. Nelson & P. M. Tuskes

  3. Department of Biological Sciences, Louisiana State University, 71115, Shreveport, Louisiana

    S. P. Lynch

Authors
  1. L. P. Brower
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  2. J. N. Seiber
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  3. C. J. Nelson
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  4. S. P. Lynch
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  5. P. M. Tuskes
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Additional information

Lepidoptera: Danaidae.

Apocynales: Asclepiadaceae.

This study was supported by N.S.F. grants DEB 75-14265 and DEB 78-10658 to Amherst College and DEB 80-40388 to the University of Florida with L.P. Brower as Principal Investigator and DEB 75-14266 and DEB 78-10659 to the University of California at Davis with J.N. Seiber as Principal Investigator.

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Brower, L.P., Seiber, J.N., Nelson, C.J. et al. 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 8, 579–633 (1982). https://doi.org/10.1007/BF00989631

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  • DOI: https://doi.org/10.1007/BF00989631

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