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Chemical defence in chewing and sucking insect herbivores: Plant-derived cardenolides in the monarch butterfly and oleander aphid

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Summary

Cardenolide sequestration by a hemimetabolous aphid and a holometabolous butterfly from the neotropical milkweed,Asclepias curassavica L., is compared. The oleander aphid,Aphis nerii B. de F., sequestered a similarly narrow range of cardenolide concentrations to the monarch butterfly,Danaus plexippus (L.), from the wide range of concentrations available in leaves of A.curassavica. However, A.nerii sequestered significantly less cardenolide (269 µg/0.1 g) thanD. plexippus (528 µg/0.1 g). The honeydew excreted by A.nerii was comprised of 46% cardenolide. The complete polarity range of 25 cardenolides detected by thin layer chromatography in A.curassavica was represented in the 17 whole aphid cardenolides and the 20 aphid honeydew cardenolides detected. D.plexippus sequestered a narrower polarity range of 11 cardenolides, having eliminated low polarity cardenolide genins and glycosides. It is suggested that these chemical differences may be related to interactions among the broad feeding tactics of sucking or chewing milkweed leaves, life history constraints of holometabolyversus hemimetaboly, the distribution of milkweed food resources in space and time, and the dynamics of natural enemies.

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References

  • Ackery PR, Vane-Wright RI (1984) Milkweed Butterflies: Their Cladistics and Biology. London: British Museum (Natural History)

    Google Scholar 

  • Arellano-G A, Glendinning JI, Brower LP (1990) Interspecific comparisons of the foraging dynamics of black-backed orioles and blackheaded grosbeaks on overwintering monarch butterflies in Mexico. In pressin Malcolm SB, Zalucki MP (eds) Biology and Conservation of the Monarch Butterfly. Los Angeles: Los Angeles County Natural History Museum

    Google Scholar 

  • Bailey MP (1974) Cardenolides (cardiac glycosides) in the food and the honeydew of the oleander aphid,Aphis nerii. Part II Biochemistry Honours thesis: University of Oxford

  • Benson JM, Seiber JN (1978) High-speed liquid chromatography of cardiac glycosides in milkweed plants and monarch butterflies. J Chromat 148:521–527

    Google Scholar 

  • Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892

    Google Scholar 

  • Blum MS, Whitman DW, Severson RF, Arrendale RF (1987) Herbivores and toxic plants: evolution of a menu of options for processing allelochemicals. Insect Sci Applic 8:459–463

    Google Scholar 

  • Boevé J-L, Pasteels JM (1985) Modes of defense in nematine sawfly larvae. J Chem Ecol 11:1019–1036

    Google Scholar 

  • Boppré M (1984) Redefining “pharmacophagy”. J Chem Ecol 10:1151–1154

    Google Scholar 

  • Boppré M (1986) Insects pharmacophagously utilizing defensive plant chemicals (pyrrolizidine alkaloids). Naturwiss 73:17–26

    Google Scholar 

  • Boppré M (1990) Lepidoptera and pyrrolizidine alkaloids: exemplification of complexity in chemical ecology. J Chem Ecol 16:165–185

    Google Scholar 

  • Botha CEJ, Malcolm SB, Evert RF (1977) An investigation of preferential feeding habit in fourAsclepiadaceae by the aphid,Aphis nerii B. de F. Protoplasma 92:1–19

    Google Scholar 

  • Brower LP (1969) Ecological chemistry. Sci Am 220:22–29

    PubMed  Google Scholar 

  • Brower LP (1984) Chemical defence in butterflies. Pp 109–134in Vane-Wright RI, Ackery PR (eds) The Biology of Butterflies. Symp R Entomol Soc Lond 11. London: Academic Press

    Google Scholar 

  • Brower LP, Calvert WH (1985) Foraging dynamics of bird predators on overwintering monarch butterflies in Mexico. Evolution 39:852–868

    Google Scholar 

  • Brower LP, Fink LS (1985) A natural toxic defense system: cardenolides in butterflies versus birds. Ann New York Acad Sci 443:171–186

    Google Scholar 

  • Brower LP, Glazier SC (1975) Localization of heart poisons in the monarch butterfly. Science 188:19–25

    Google Scholar 

  • Brower LP, Ryerson WN, Coppinger LL, Glazier SC (1968) Ecological chemistry and the palatability spectrum. Science 161:1349–1351

    Google Scholar 

  • Brower LP, Seiber JN, Nelson CJ, Lynch SP, Tuskes PM (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 8:579–633

    Google Scholar 

  • Brower LP, Horner BE, Marty MA, Moffitt CM, Villa-R B (1985) Mice (Peromyscus maniculatus, P. spicilegus, andMicrotus mexicanus) as predators of overwintering monarch butterflies (Danaus plexippus) in Mexico. Biotropica 17:89–99

    Google Scholar 

  • Brower LP, Nelson CJ, Seiber JN, Fink LS, Bond C (1988) Exaptation as an alternative to coevolution in the cardenolide-based chemical defense of monarch butterflies (Danaus plexippus L.) against avian predators. Pp 447–475in Spencer KC (ed) Chemical Mediation of Coevolution. San Diego: Academic Press

    Google Scholar 

  • Brown KS Jr (1984a) Adult-obtained pyrrolizidine alkaloids defend ithomiine butterflies against a spider predator. Nature 309:707–709

    Google Scholar 

  • Brown KS Jr (1984b) Chemical ecology of dehydropyrrolizidine alkaloids in adult Ithomiinae (Lepidoptera: Nymphalidae). Rev Brasil Biol 44:435–460

    Google Scholar 

  • Brown KS Jr (1987) Chemistry at the Solanaceae/Ithomiinae interface. Ann Miss Bot Gard 74:359–397

    Google Scholar 

  • Brown KS Jr, Cameron DW, Weiss U (1969) Chemical constituents of the bright orange aphidAphis nerii Fonscolombe. I Neriaphin and 6-hy-droxymusizin 8-O-β-D-glucoside. Tetrahedron Lett 6:471–476

    PubMed  Google Scholar 

  • Calvert WH, Hedrick HE, Brower LP (1979) Mortality of the monarch butterfly (Danaus plexippus L.): avian predation at five overwintering sites in Mexico. Science 204:847–851

    Google Scholar 

  • Cohen JA (1985) Differences and similarities in cardenolide contents of queen and monarch butterflies in Florida and their ecological and evolutionary implications. J Chem Ecol 11:85–103

    Google Scholar 

  • Dixon CA, Erickson JM, Kellett DN, Rothschild DN (1978) Some adaptations betweenDanaus plexippus and its food plant, with notes onDanaus chrysippus andEuploea core (Insecta: Lepidoptera). J Zool Lond 185:437–467

    Google Scholar 

  • Duffey SS (1980) Sequestration of plant natural products by insects. Ann Rev Entomol 25:447–477

    Google Scholar 

  • Duffey SS, Scudder GGE (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 

  • Dussourd DE, Eisner T (1987) Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237:898–901

    PubMed  Google Scholar 

  • Dussourd DE, Ubik K, Harvis C, Resch J, Meinwald J, Eisner T (1988) Biparental defensive endowment of eggs with acquired plant alkaloid in the mothUtetheisa ornatrix. Proc Natl Acad Sci USA 85:5992–5996

    PubMed  Google Scholar 

  • Fink LS, Brower LP (1981) Birds can overcome the cardenolide defence of monarch butterflies in Mexico. Nature 291:67–70

    Google Scholar 

  • Fink LS, Brower LP, Waide RB, Spitzer PR (1983) Overwintering monarch butterflies as food for insectivorous birds in Mexico. Biotropica 15:151–153

    Google Scholar 

  • Glendinning JI (1990) Comparative feeding responses of the micePeromyscus melanotis, P. aztecus hylocetes, Reithrodontomys sumichrasti, andMicrotus mexicanus salvus, to overwintering monarch butterflies in Mexico. In pressin Malcolm SB, Zalucki MP (eds) Biology and Conservation of the Monarch Butterfly. Los Angeles: Los Angeles County Natural History Museum

    Google Scholar 

  • Glendinning JI, Alonso Mejia A, Brower LP (1988) Behavioral and ecological interactions of foraging mice (Peromyscus melanotis) with overwintering monarch butterflies (Danaus plexippus) in Mexico. Oecologia 75:222–227

    Google Scholar 

  • Groeters F (1990) Geographic and clonal variation in the milkweed-oleander aphid,Aphis nerii Fonscolombe (Homoptera: Aphididae), for response to crowding, life history, and morphology in relation to host plant permanence. Evol Ecol (in press)

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

    Google Scholar 

  • Isman MB, Duffey SS, Scudder GGE (1977) 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 

  • Jones CG, Hess TA, Whitman DW, Silk PJ, Blum MS (1986) Idiosyncratic variation in chemical defenses among individual generalist grasshoppers. J Chem Ecol 12:749–761

    Google Scholar 

  • Jones CG, Hess TA, Whitman DW, Silk PJ, Blum MS (1987) Effects of diet breadth on autogenous chemical defense of a generalist grasshopper. J Chem Ecol 13:283–297

    Google Scholar 

  • Jones CG, Whitman DW, Silk PJ, Blum MS (1988) Diet breadth and insect chemical defenses: a generalist grasshopper and general hypotheses. Pp 477–512in Spencer KC (ed) Chemical Mediation of Coevolution. San Diego: Academic Press

    Google Scholar 

  • Jones CG, Whitman DW, Compton SJ, Silk PJ, Blum MS (1989) Reduction in diet breadth results in sequestration of plant chemicals and increases efficacy of chemical defense in a generalist grasshopper. J Chem Ecol 15:1811–1822

    Google Scholar 

  • Lee SM, Seiber JN (1983) Biosynthetic preparation of cardenolides from [1-14C]acetic acid by stem discs of the milkweedAsclepias curassavica. Phytochemistry 22:923–927

    Google Scholar 

  • Malcolm SB (1981) Defensive use of plant-derived cardenolides byAphis nerii B. de F. againsf predation. University of Oxford: D. Phil. thesis

  • Malcolm SB (1986) Aposematism in a soft-bodied insect: a case for kin selection. Behav Ecol Sociobiol 18:387–393

    Google Scholar 

  • Malcolm SB (1989) Disruption of web structure and predatory behavior of a spider by plant-derived chemical defenses of an aposematic aphid. J Chem Ecol 15:1699–1716

    Google Scholar 

  • Malcolm SB, Brower LP (1986) Selective oviposition by monarch butterflies (Danaus plexippus L.) in a mixed stand ofAsclepias curassavica L., andA. incarnata L. in south Florida. J Lep Soc 40(4):255–263

    Google Scholar 

  • Malcolm SB, Brower LP (1989) Evolutionary and ecological implications of cardenolide sequestration in the monarch butterfly. Experientia 45:284–295

    Google Scholar 

  • Malcolm SB, Cockrell BJ, Brower LP (1989) Cardenolide fingerprint of monarch butterflies reared on common milkweed,Asclepias syriaca L. J Chem Ecol 15:819–853

    Google Scholar 

  • Moore LV, Scudder GGE (1985) Selective sequestration of milkweed (Asclepias sp.) cardenolides inOncopeltus fasciatus (Dallas)(Hemiptera: Lygaeidae). J Chem Ecol 11:667–687

    Google Scholar 

  • Nelson CJ, Seiber JN, Brower LP (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 

  • Nishida R, Fukami H (1989) Host plant iridoid-based chemical defense of an aphid,Acyrthosiphon nipponicus, against ladybird beetles. J Chem Ecol 15:1837–1845

    Google Scholar 

  • Oyeyele SO, Zalucki MP (1990) Cardiac glycosides and oviposition byDanaus plexippus onAsclepias fruticosa in south-east Queensland (Australia), with notes on the effect of plant nitrogen content. Ecol Entomol 15 (in press)

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

    PubMed  Google Scholar 

  • Pasteels JM (1978) Apterous and brachypterous coccinellids at the end of the food chain,Cionura erecta (Asclepiadaceae) —Aphis nerii. Entomol exp appl 24:379–384

    Google Scholar 

  • Reichstein T (1967) Cardenolide (herzwirksame Glykoside) als Abwehrstoffe bei Insekten. Naturw Rdsch Stuttg 20:499–511

    Google Scholar 

  • Reichstein T, von Euw J, Parsons JA, Rothschild M (1968) Heart poisons in the monarch butterfly. Science 161:861–866

    PubMed  Google Scholar 

  • Rhoades DF (1983) Herbivore population dynamics and plant chemistry. Pp 155–222in Denno RF, McClure MS (eds) Variable Plants and Herbivores in Natural and Managed Systems. New York: Academic Press

    Google Scholar 

  • Roeske CN, Seiber JN, Brower LP, Moffitt CM (1976) Milkweed cardenolides and their comparative processing by monarch butterflies (Danaus plexippus L.). Recent Adv Phytochem 10:93–167

    Google Scholar 

  • Rothschild M (1973) Secondary plant substances and warning colouration in insects. Pp 59–83in van Emden HF (ed) Insect/Plant Relationships. Symp R Entomol Soc Lond 6. Oxford: Blackwell Scientific Publications

    Google Scholar 

  • Rothschild M, Reichstein T (1976) Some problems associated with the storage of cardiac glycosides by insects. Nova Acta Leopoldina Suppl 7:507–550

    Google Scholar 

  • Rothschild M, Von Euw J, Reichstein T (1970) Cardiac glycosides in the oleander aphidAphis nerii. J Insect Physiol 16:1141–1145

    PubMed  Google Scholar 

  • Rothschild M, Von Euw J, Reichstein T, Smith DAS, Pierre J (1975) Cardenolide storage inDanaus chrysippus (L.) with additional notes onD. plexippus (L.). Proc R Soc Lond B 190:1–31

    Google Scholar 

  • Scudder GGE, Duffey SS (1972) Cardiac glycosides in the Lygaeinae (Hemiptera: Lygaeidae). Can J Zool 50:35–42

    Google Scholar 

  • Scudder GGE, Moore LV, Isman MB (1986) Sequestration of cardenolides inOncopeltus fasciatus: morphological and physiological adaptations. J Chem Ecol 12:1171–1187

    Google Scholar 

  • Seiber JN, Tuskes PM, Brower LP, Nelson CJ (1980) Pharmacodynamics of some individual milkweed cardenolides fed to larvae of the monarch butterfly (Danaus plexippus L.). J Chem Ecol 6:321–339

    Google Scholar 

  • Seiber JN, Nelson CJ, Lee SM (1982) Cardenolides in the latex and leaves of sevenAsclepias species andCalotropis procera. Phytochemistry 21:2343–2348

    Google Scholar 

  • Seiber JN, Lee SM, Benson JM (1983) Cardiac glycosides (cardenolides) in species ofAsclepias (Asclepiadaceae). Pp 43–83in Keeler RF, Tu AT (eds) Handbook of Natural Toxins. Vol 1. Plant and Fungal Toxins. New York, Basel: Marcel Dekker

    Google Scholar 

  • Strong DR, Lawton JH, Southwood TRE (1984) Insects on Plants: community patterns and mechanisms. Oxford: Blackwell Scientific Publications

    Google Scholar 

  • Tahsler BD (1975) The distribution of cardenolides inAsclepias curassavica andA. nivea and its effect on the uptake of cardenolides by monarch nutterfly larvae: implications for the cardenolide dynamics of natural monarch populations. Amherst College, Massachusetts: Honors Biology thesis.

  • Trigo JR, Brown KS Jr (1990) Variation of pyrrolizidine alkaloids in Ithomiinae: a comparative study between species feeding on Apocynaceae and Solanaceae. Chemoecology 1:22–29

    Google Scholar 

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

    Google Scholar 

  • Vasconcellos-Neto J, Lewinsohn TM (1984) Discrimination and release of unpalatable butterflies byNephila clavipes, a neotropical orb-weaving spider. Ecol Entomol 9:337–344

    Google Scholar 

  • Whitman DW (1988) Allelochemical interactions among plants, herbivores, and their predators. Pp 11–64in Barbosa P, Letourneau DK (eds) Novel Aspects of Insect-Plant Interactions. New York: John Wiley & Sons

    Google Scholar 

  • Wiklund C, Järvi T (1982) Survival of distasteful insects after being attacked by naive birds: a reappraisal of the theory of aposematic coloration evolving through individual selection. Evolution 36:998–1002

    Google Scholar 

  • Wink M, Römer P (1986) Acquired toxicity — the advantages of specializing on alkaloid-rich lupins toMacrosiphon albifrons (Aphidae). Naturwissenschaften 73:210–212

    Google Scholar 

  • Wink M, Hartmann T, White L, Rheinheimer J (1982) Interrelationship between quinolizidine alkaloid producing legumes and infesting insects: exploitation of the alkaloid-containing phloem sap ofCytisus scoparius by the broom aphidAphis cytisorum. Z Naturforsch 37c:1081–1086

    Google Scholar 

  • Young AM (1982) An evolutionary-ecological model of the evolution of migratory behavior in the monarch butterfly, and its absence in the queen butterfly. Acta Biotheoretica 31:219–237

    Google Scholar 

  • Zalucki MP, Brower LP, Malcolm SB (1990) Oviposition byDanaus plexippus in relation to cardenolide content of threeAsclepias species in the southeastern U.S.A. Ecol Entomol 15 (in press)

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  1. Stephen B. Malcolm

    Present address: Department of Pure and Applied Biology, Imperial College at Silwood Park, SL5 7PY, Ascot, Berks, United Kingdom

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

    Stephen B. Malcolm

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Malcolm, S.B. Chemical defence in chewing and sucking insect herbivores: Plant-derived cardenolides in the monarch butterfly and oleander aphid. Chemoecology 1, 12–21 (1990). https://doi.org/10.1007/BF01240581

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