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Sequestration of cardenolides inOncopeltus fasciatus: Morphological and physiological adaptations

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Abstract

The morphological and physiological adaptations associated with sequestration of cardenolides by the lygaeidOncopeltus fasciatus are summarized and discussed. Cardenolides are efficiently accumulated inO. fasciatus; however, the insect does not appear to suffer any physiological cost as a result of handling large amounts of these plant toxins. Morphological adaptations of the insect include a modified integument composed of a double layered epidermis with an inner layer (the dorsolateral space) specialized for cardenolide storage. Special weak areas of the cuticle are found on both the thorax and abdomen, which rupture when the insect is squeezed, resulting in the cardenolide-rich contents of the inner epidermal layer being released onto the body surface in the form of discrete spherical droplets. Physiological adaptations include selective sequestration of food plant cardenolides, concentration of cardenolides in the dorsolateral space, passive uptake of cardenolides at the gut and dorsolateral space requiring little energy output, reabsorption of secreted cardenolides by the Malpighian tubules, high in vivo tolerance to cardenolides, and the presence of cardenolide-resistant Na,K-ATPases.

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References

  • Abushama, F.T., andAhmed, A.A. 1976. Food-plant preference and defense mechanisms in the lygaeid bugSpilostethus pandurus (Scop.).Z Angew. Entomol. 80:206–213.

    Google Scholar 

  • Akera, T. 1977. Membrane adenosinetriphosphatase: A digitalis receptor?Science 198:569–574.

    Google Scholar 

  • Ashurst, D.E. 1968. The connective tissues of insects.Annu. Rev. Entomol. 13:45–74.

    Google Scholar 

  • Baggini, A., Bernardi, R., Casnati, G., Pavan, M., andRicca, A. 1966. Richerche sulle secrezioni difensive di insetti Emitteri Eterotteri (Hem:Heteroptera).Eos 42:7–26.

    Google Scholar 

  • Baker, R.M., Brunette, D.M., Mankovitz, R., Thompson, L.H., Whitmore, G.F., Siminovitch, L., andTill, J.E. 1974. Ouabain-resistant mutants of mouse and hamster cells in culture.Cell 1:9–21.

    Google Scholar 

  • Berenbaum, M.R., andMiliczky, E. 1984. Mantids and milkweed bugs: Efficacy of aposematic coloration against invertebrate predators.Am. Midl. Nat. 111:64–68.

    Google Scholar 

  • Blum, M.S. 1981. Chemical Defenses of Arthropods. Academic Press, New York. 562 pp.

    Google Scholar 

  • Blum, M.S. 1983. Detoxication, deactivation, and utilization of plant compounds of insects, chapter 15, pp. 265–275,in P.A. Hedin (ed.). Plant Resistance to Insects. American Chemical Society Symposium Series No. 208.

  • Bodemann, H.H. 1981. The current concept for the cardiac glycoside receptor.Clin. Cardiol. 4:223–228.

    Google Scholar 

  • Bongers, J. 1969. Zur Frage der Wirtsspezifitat beiOncopeltus fasciatus (Heteroptera: Lygaeidae).Entomol. Exp. Appl. 12:147–156.

    Google Scholar 

  • Brower, L.P. 1969. Ecological chemistry.Sci. Am. 220(2):22–29.

    Google Scholar 

  • Brower, L.P., andBrower, J.V.z. 1964. Birds, butterflies, and plant poisons: A study in ecological chemistry.Zoologica (N.Y.) 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., 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 butterfliesDanaus plexippus reared on the milkweed,Asclepias eriocarpa in California.J. Chem. Ecol. 8:579–633.

    Google Scholar 

  • Brower, L.P., Seiber, J.N., Nelson, C.J., Lynch, S.P., andHolland, M.M. 1984. Plant-determined variation in the cardenolide content, thin-layer chromatography profiles, and emetic potency of monarch butterflies,Danaus plexippus L. reared on milkweed plants in California: 2.Asclepias speciosa.J. Chem. Ecol. 10:601–639.

    Google Scholar 

  • Calam, D.H., andYoudeowei, A. 1968. Identification and functions of secretions from the posterior scent gland of fifth instar larva of the bugDysdercus intermedius.J. Insect Physiol. 14:1147–1158.

    Google Scholar 

  • Chaplin, S.J., andChaplin, S.B. 1981. Growth dynamics of a specialized milkweed seed feeder (Oncopeltus fasciatus) on seeds of familiar and unfamiliar milkweeds (Asclepias sp.).Entomol. Exp. Appl. 29:345–356.

    Google Scholar 

  • Cohen, J.A. 1985. Differences and similarities in cardenolide contents of queen and monarch butterflies in Florida and their ecological and evolutionary implications.J. Chem. Ecol. 11(1):85–103.

    Google Scholar 

  • Cohen, J.A., andBrower, L.P. 1983. Cardenolide sequestration by the dogbane tiger moth (Cycnia tenera; Arctiidae).J. Chem. Ecol. 9:521–532.

    Google Scholar 

  • Dazzini, V.M., andPavan, M. 1978. Scent glands and defensive functions in Rhynchota.Publ. 1st Entomol. Univ. Pavia 5:1–46.

    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 

  • Eggermann, W., andBongers, J. 1971. Wasser- und Nahrungsaufnahme an Pflanzen unter besonderer Berücksichtgung der Wirtsspezifität vonOncopeltus fasciatus Dallas.Oecologia 6:303–317.

    Google Scholar 

  • Eggermann, W., andBongers, J. 1972. Host selection ofOncopeltus fasciatus Dall. (Heteroptera: Lygaeidae): Glycosides of Asclepiadaceae the chemical basis for host specificity.Oecologia 9:363–370.

    Google Scholar 

  • Feir, D. 1974.Oncopeltus fasciatus: A research animal.Annu. Rev. Entomol. 19:81–96.

    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 

  • Frings, H., andLittle, F. 1955. Peanuts as a substitute food for the large milkweed bug,Oncopeltus fasciatus.J. Econ. Entomol. 50:363–364.

    Google Scholar 

  • Games, D.E., andStaddon, B.W. 1973a. Chemical expression of a sexual dimorphism in the tubular scent glands of the milkweed bugOncopeltus fasciatus (Dallas) (Heteroptera; Lygaeidae).Experientia 29:532–533.

    Google Scholar 

  • Games, D.E., andStaddon, B.W. 1973b. Composition of scents from the larva of the milkweed bugOncopeltus fasciatus.J. Insect Physiol. 19:1527–1532.

    Google Scholar 

  • Gelperin, A. 1968. Feeding behaviour of the praying mantis: A learned modification.Nature 219:399–400.

    Google Scholar 

  • Gordon, H.T., andLoher, W. 1968. Egg production and male activation in new laboratory strains of the large milkweed bug,Oncopeltus fasciatus.Ann. Entomol. Soc. Am. 61:1573–1578.

    Google Scholar 

  • Guthrie, D.M., andTindall, A.R. 1968. The Biology of the Cockroach. Edward Arnold, London.

    Google Scholar 

  • Henrici, H. 1938. Die Hautdrüsen der Landwanzen (Geocorisae), ihre mikroskopische Anatomie, ihre Histologie und Entwicklung. Teil I. Die abdominalen Stinkdrüsen, die Drüsenpakete und die zerstreuten Hautdrüsen.Zool. Jahrb. Anat. 65:141–228.

    Google Scholar 

  • Henrici, H. 1939. Die Hautdrüsen der Landwanzen (Geocorisae), ihre mikroskopische Anatomie, ihre Histologie und Entwicklung. Teil II. Die thorakalen Stinkdrüsen.Zool. Jahrb. Anat. 66:371–402.

    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. 1979. Cardenolide content of Lygaeid bugs onAsclepias curassavica in Costa Rica.Biotropica 11:78–79.

    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 (Asclelpias spp.).Can. J. Zool. 55:1024–1028.

    Google Scholar 

  • Johansson, A.S. 1957. The functional anatomy of the metathoracic scent glands of the milkweed bug,Oncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae).Norsk. Entomol. Tidskr. 10:95–109.

    Google Scholar 

  • Jones, C.G., Hoggard, M.P., andBlum, M.S. 1983. Is sequestration structure-specific in the milkweed bug,Oncopeltus fasciatus?Comp. Biochem. Physiol. C 76:283–284.

    Google Scholar 

  • Jones, F.M. 1932. Insect coloration and the relative acceptability of insects to birds.Trans. R. Entomol. Soc. London 80:345–385.

    Google Scholar 

  • Jones, F.M. 1934. Further experiments on coloration and relative acceptability of insects to birds.Trans. R. Entomol. Soc. London 82:443–453.

    Google Scholar 

  • Kilby, B.A. 1963. The biochemistry of the insect fat body, pp. 111–174,in, J.W.L. Beament, J.E. Treherne and V.B. Wigglesworth (eds.). Advances in Physiology, Vol. 7. Academic Press, London.

    Google Scholar 

  • Klausner, E., Miller, E.R., andDingle, H. 1980.Nerium oleander as an alternative host plant for south Florida milkweed bugs,Oncopeltus fasciatus.Ecol. Entomol. 5:137–142.

    Google Scholar 

  • Landolph, J.R., Bhatt, R.S., Telker, N., andHeidelberger, C. 1980. Comparison of adriamycin and ouabain-induced cytotoxicity and inhibition of86rubidium transport in wild-type and ouabain-resistant C3H/10T1/2 mouse fibroblasts.Cancer Res. 40:4581–4588.

    Google Scholar 

  • Levey, B. 1983. Plant allelochemicals and the evolution of host-plant relationships in the genusSpilostethus. PhD thesis. University of Witwatersrand, Johannesburg. 205 pp.

    Google Scholar 

  • Mankovitz, R., Buchwald, M., andBaker, R.M. 1974. Isolation of ouabain-resistant human diploid fibroblasts.Cell 3:221–226.

    Google Scholar 

  • Meredith, J., Moore, L., andScudder, G.G.E. 1984. The excretion of ouabain by the Malpighian tubules ofO. fasciatus.Am. J. Physiol. 246(Regulatory Integrative Comp. Physiol. 15):R705-R715.

    Google Scholar 

  • Moore, L.V., andScudder, G.G.E. 1985. Selective sequestration of milkweed (Asclepias sp.) cardenolides inOncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae).J. Chem. Ecol. 5:667–687.

    Google Scholar 

  • Moore, L.V., andScudder, G.G.E. 1986. Ouabain-resistant Na,K-ATPases and cardenolide tolerance in the large milkweed bug,Oncopeltus fasciatus.J. Insect Physiol. 1:27–33.

    Google Scholar 

  • Neville, A.C. 1975. Biology of the Arthropod Cuticle. Springer-Verlag, New York.

    Google Scholar 

  • Nishio, S. 1980. The fates and adaptive significance of cardenolides sequestered by larvae ofDanaus plexippus (L.) andCycnia inopinatus (Hy. Edwards). PhD thesis, University of Georgia, Athens, Georgia. 119 pp.

    Google Scholar 

  • Nishio, S., Blum, M.S., andTakahashi, S. 1983. Intraplant distribution of cardenolides inAsdepias humistrata (Asclepiadaceae), with additional notes on their fates inTetraopes melanurus (Coleoptera: Cerambycidae) andRhyssomatus lineaticollis (Coleoptera: Curculionidae).Mem. Coll. Agric., Kyoto Univ. 122:3–52.

    Google Scholar 

  • Remold, H. 1962. Über die biologische Bedeutung der Duftdrüsen bei den Landwanzen (Geocorisae).Z. Vergl. Physiol. 45:636–694.

    Google Scholar 

  • Remold, H. 1963. Scent-glands of land-bugs, their physiology and biological function.Nature 198:764–768.

    Google Scholar 

  • Richards, A.G. 1951. The Integument of Arthropods. The Chemical Components and Their Properties, the Anatomy and Development, and the Permeability. University of Minnesota Press, Minneapolis.

    Google Scholar 

  • Robbins, A.R., andBaker, R.M. 1977. (Na,K)-ATPase activity in membrane preparations of ouabain-resistant HeLa cells.Biochemistry 16:5163–5168.

    Google Scholar 

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

    Google Scholar 

  • Rothschild, M. 1966. Experiments with captive predators and the poisonous grasshopperPoekilocerus bufonis (Klug).Proc. R. Entomol. Soc. London (C) 31:32.

    Google Scholar 

  • Rothschild, M. 1972. Secondary plant substances and warning coloration in insects.Symp. R. Entomol. Soc. London 6:59–83.

    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., von Euw, J., andReichstein, T. 1970. Cardiac glycosides in the oleander aphid,Aphis nerii.J. Insect Physiol. 16:1141–1145.

    Google Scholar 

  • Rothschild, M., von Euw, J., andReichstein, J. 1973. Cardiac glycosides in a scale insect (Aspidiotus), a lady bird (Coccinella) and a lacewing (Chrysopa).J. Entomol. 48:89–90.

    Google Scholar 

  • Sauer, D., andFeir, D. 1972. Field observations on predation on the large milkweed bug,Oncopeltus fasciatus.Environ. Entomol. 1:268.

    Google Scholar 

  • Schaefer, C.W. 1972. Degree of metathoracic scent-gland development in the trichophorous Heteroptera (Hemiptera).Ann. Entomol. Soc. Am. 65:810–821.

    Google Scholar 

  • Schwalb, H., Dickstein, Y., andHeller, M. 1982. Interactions of cardiac glycosides with cardiac cells. III. Alterations in the sensitivity of (Na+ +K+)-ATPase to inhibition by ouabain in rat hearts.Biochim. Biophys. Acta 689:241–248.

    Google Scholar 

  • Scudder, G.G.E., andDuffey, S.S. 1972. Cardiac glycosides in the Lygaeinae (Hemiptera: Lygaeidae).Can. J. Zool. 50:35–42.

    Google Scholar 

  • Scudder, G.G.E., andMeredith, J. 1982a. Morphological basis of cardiac glycoside sequestration byOncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae).Zoomorphology (Berlin) 99:87–101.

    Google Scholar 

  • Scudder, G.G.E., andMeredith, J. 1982b. The permeability of the midgut of three insects to cardiac glycosides.J. Insect Physiol. 28:689–694.

    Google Scholar 

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

    Google Scholar 

  • Sillén-Tullberg, B., Wiklund, C., andJärvi, T. 1982. Aposematic coloration in adults and larvae ofLygaeus equestris and its bearing on Mullerian mimicry: An experimental study on predation on living bugs by the great titParus major.Oikos 39:131–136.

    Google Scholar 

  • Staddon, B.W. 1979. The scent glands of Heteroptera.Adv. Insect Physiol. 14:351–418.

    Google Scholar 

  • Tsuyuki, T., Ogata, Y., Yamamoto, I., andShimi, K. 1965. Stink bug aldehydes.Agric. Biol. Chem. 29:419–427.

    Google Scholar 

  • Vaughan, F.A. 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 

  • 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 

  • von Euw, J., Reichstein, T., andRothschild, M. 1971. Heart poisons (cardiac glycosides) in the Lygaeid bugsCaenocoris nerii andSpilostethus pandurus.Insect Biochem. 1:373–384.

    Google Scholar 

  • Weatherston, J., andPercy, I.E. 1978. Venoms of Rhyncota (Hemiptera). Arthropod Venoms.Hand. Exp. Pharmacol 48:489–509.

    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 

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Authors and Affiliations

  1. Department of Zoology, University of British Columbia, V6T 1W5, Vancouver, Canada

    G. G. E. Scudder & L. V. Moore

  2. Department of Plant Science, University of British Columbia, V6T 1W5, Vancouver, Canada

    M. B. Isman

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  1. G. G. E. Scudder
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Hemiptera-Heteroptera: Lygaeidae.

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Scudder, G.G.E., Moore, L.V. & Isman, M.B. Sequestration of cardenolides inOncopeltus fasciatus: Morphological and physiological adaptations. J Chem Ecol 12, 1171–1187 (1986). https://doi.org/10.1007/BF01639003

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