Journal of Chemical Ecology

, Volume 12, Issue 5, pp 1171–1187 | Cite as

Sequestration of cardenolides inOncopeltus fasciatus: Morphological and physiological adaptations

  • G. G. E. Scudder
  • L. V. Moore
  • M. B. Isman
Article

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.

Key words

Hemiptera Heteroptera Lygaeidae Oncopeltus fasciatus Asclepiadaceae cardenolides sequestration morphological adaptations physiological adaptations 

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References

  1. 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
  2. Akera, T. 1977. Membrane adenosinetriphosphatase: A digitalis receptor?Science 198:569–574.Google Scholar
  3. Ashurst, D.E. 1968. The connective tissues of insects.Annu. Rev. Entomol. 13:45–74.Google Scholar
  4. 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
  5. 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
  6. 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
  7. Blum, M.S. 1981. Chemical Defenses of Arthropods. Academic Press, New York. 562 pp.Google Scholar
  8. 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.Google Scholar
  9. Bodemann, H.H. 1981. The current concept for the cardiac glycoside receptor.Clin. Cardiol. 4:223–228.Google Scholar
  10. Bongers, J. 1969. Zur Frage der Wirtsspezifitat beiOncopeltus fasciatus (Heteroptera: Lygaeidae).Entomol. Exp. Appl. 12:147–156.Google Scholar
  11. Brower, L.P. 1969. Ecological chemistry.Sci. Am. 220(2):22–29.Google Scholar
  12. 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
  13. Brower, L.P., andGlazier, S.C. 1975. Localization of heart poisons in the monarch butterfly.Science 188:19–25.Google Scholar
  14. Brower, L.P., andMoffitt, C.M. 1974. Palatability dynamics of cardenolides in the monarch butterfly.Nature 249:280–283.Google Scholar
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. Dazzini, V.M., andPavan, M. 1978. Scent glands and defensive functions in Rhynchota.Publ. 1st Entomol. Univ. Pavia 5:1–46.Google Scholar
  22. 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
  23. 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
  24. Eggermann, W., andBongers, J. 1971. Wasser- und Nahrungsaufnahme an Pflanzen unter besonderer Berücksichtgung der Wirtsspezifität vonOncopeltus fasciatus Dallas.Oecologia 6:303–317.Google Scholar
  25. 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
  26. Feir, D. 1974.Oncopeltus fasciatus: A research animal.Annu. Rev. Entomol. 19:81–96.Google Scholar
  27. 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
  28. 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
  29. 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
  30. 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
  31. Gelperin, A. 1968. Feeding behaviour of the praying mantis: A learned modification.Nature 219:399–400.Google Scholar
  32. 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
  33. Guthrie, D.M., andTindall, A.R. 1968. The Biology of the Cockroach. Edward Arnold, London.Google Scholar
  34. 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
  35. 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
  36. 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
  37. Isman, M.B. 1979. Cardenolide content of Lygaeid bugs onAsclepias curassavica in Costa Rica.Biotropica 11:78–79.Google Scholar
  38. 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
  39. 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
  40. 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
  41. 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
  42. Jones, F.M. 1932. Insect coloration and the relative acceptability of insects to birds.Trans. R. Entomol. Soc. London 80:345–385.Google Scholar
  43. 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
  44. 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
  45. 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
  46. 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
  47. 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
  48. Mankovitz, R., Buchwald, M., andBaker, R.M. 1974. Isolation of ouabain-resistant human diploid fibroblasts.Cell 3:221–226.Google Scholar
  49. 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
  50. 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
  51. 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
  52. Neville, A.C. 1975. Biology of the Arthropod Cuticle. Springer-Verlag, New York.Google Scholar
  53. 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
  54. 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
  55. Remold, H. 1962. Über die biologische Bedeutung der Duftdrüsen bei den Landwanzen (Geocorisae).Z. Vergl. Physiol. 45:636–694.Google Scholar
  56. Remold, H. 1963. Scent-glands of land-bugs, their physiology and biological function.Nature 198:764–768.Google Scholar
  57. 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
  58. 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
  59. 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
  60. Rothschild, M. 1966. Experiments with captive predators and the poisonous grasshopperPoekilocerus bufonis (Klug).Proc. R. Entomol. Soc. London (C) 31:32.Google Scholar
  61. Rothschild, M. 1972. Secondary plant substances and warning coloration in insects.Symp. R. Entomol. Soc. London 6:59–83.Google Scholar
  62. 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
  63. Rothschild, M., von Euw, J., andReichstein, T. 1970. Cardiac glycosides in the oleander aphid,Aphis nerii.J. Insect Physiol. 16:1141–1145.Google Scholar
  64. 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
  65. Sauer, D., andFeir, D. 1972. Field observations on predation on the large milkweed bug,Oncopeltus fasciatus.Environ. Entomol. 1:268.Google Scholar
  66. Schaefer, C.W. 1972. Degree of metathoracic scent-gland development in the trichophorous Heteroptera (Hemiptera).Ann. Entomol. Soc. Am. 65:810–821.Google Scholar
  67. 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
  68. Scudder, G.G.E., andDuffey, S.S. 1972. Cardiac glycosides in the Lygaeinae (Hemiptera: Lygaeidae).Can. J. Zool. 50:35–42.Google Scholar
  69. 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
  70. 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
  71. 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
  72. 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
  73. Staddon, B.W. 1979. The scent glands of Heteroptera.Adv. Insect Physiol. 14:351–418.Google Scholar
  74. Tsuyuki, T., Ogata, Y., Yamamoto, I., andShimi, K. 1965. Stink bug aldehydes.Agric. Biol. Chem. 29:419–427.Google Scholar
  75. 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
  76. 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
  77. 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
  78. 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
  79. Weatherston, J., andPercy, I.E. 1978. Venoms of Rhyncota (Hemiptera). Arthropod Venoms.Hand. Exp. Pharmacol 48:489–509.Google Scholar
  80. 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

Copyright information

© Plenum Publishing Corporation 1986

Authors and Affiliations

  • G. G. E. Scudder
    • 1
  • L. V. Moore
    • 1
  • M. B. Isman
    • 2
  1. 1.Department of ZoologyUniversity of British ColumbiaVancouverCanada
  2. 2.Department of Plant ScienceUniversity of British ColumbiaVancouverCanada

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