Journal of Chemical Ecology

, Volume 17, Issue 8, pp 1593–1610 | Cite as

Palatability of aposematic queen butterflies (Danaus gilippus) feeding onSarcostemma clausum (Asclepiadaceae) in Florida

  • David B. Ritland
Article

Abstract

Queen butterflies (Danaus gilippus) are generally considered unpalatable to predators because they sequester and store toxic cardenolides from their larval food plants. However, a major queen food plant in Florida, the asclepiadaceous vineSarcostemma clausum, is shown here to be a very poor cardenolide source, and queens reared on this plant contain no detectable cardenolide. A direct evaluation of queen palatability using red-winged blackbirds indicates thatS. clausum-reared butterflies are essentially palatable to these predators (85% of abdomens entirely eaten), indicating little protection from either cardenolides, other sequestered phytochemicals, or de novo defensive compounds. Wild-caught queens that presumably fed as larvae uponS. clausum and also had access to adult-obtained chemicals, such as pyrrolizidine alkaloids (PAs), were relatively palatable as well (77% of abdomens eaten); they did not differ significantly in palatability from the labreared butterflies. Together, these findings suggest that; (1)S. clausumfed queens are poorly defended against some avian predators, and (2) for the particular queen sample examined, PAs do not contribute substantially to unpalatability. The discovery thatS. clausum-feeding queens are essentially palatable is of additional significance because it compels a reassessment of the classic mimicry relationship between queen and viceroy butterflies. Viceroys have been shown recently to be moderately unpalatable; therefore, the established roles of model and mimic may be reversed in some cases.

Key Words

Chemical defense mimicry cardenolides pyrrolizidine alkaloids Asclepiadaceae Lepidoptera Danainae Danaus gilippus Limenitis archippus Sarcostemma 

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References

  1. Abisch, E., andReichstein, T. 1962. Orientierende chemische Untersuchung einiger Asclepiadaceen und Periplocaceen.Helv. Chim. Acta 45:2090–2116.Google Scholar
  2. Ackery, P.R., andVane-Wright, R.I. 1984. Milkweed Butterflies: Their Cladistics and Biology. Cornell University Press for the British Museum (Natural History), Ithaca, New York.Google Scholar
  3. Boppré, M. 1984. Chemically mediated interactions between butterflies, pp. 259–275,in R.I. Vane-Wright and P.R. Ackery (eds.). The Biology of Butterflies. Academic Press, London.Google Scholar
  4. Bowers, M.D. 1980. Unpalatability as a defense strategy ofEuphydryas phaeton (Lepidoptera: Nymphalidae).Evolution 34:586–600.Google Scholar
  5. Bowers, M.D. 1981. Unpalatability as a defense strategy of western checkerspot butterflies (Euphydryas Scudder, Nymphalidae).Evolution 35:367–375.Google Scholar
  6. Brower, J.V.Z. 1958a. Experimental studies of mimicry in some North American butterflies. I. The Monarch,Danaus plexippus and Viceroy,Limenitis archippus.Evolution 12:32–47.Google Scholar
  7. Brower, J.V.Z. 1958b. Experimental studies of mimicry in some North American butterflies. III.Danaus gilippus berenice andLimenitis archippus floridensis.Evolution 12:273–285.Google Scholar
  8. Brower, L.P. 1969. Ecological chemistry.Sci. Am. 220:22–29.PubMedGoogle Scholar
  9. Brower, L.P. 1984. Chemical defence in butterflies, pp. 109–134,in R.I. Vane-Wright and P.R. Ackery (eds.). The Biology of Butterflies. Academic Press, London.Google Scholar
  10. Brower, L.P., Brower, J.V.Z., andCranston, F.P. 1965. Courtship behaviour of the queen butterfly,Danaus gilippus berenice (Cramer).Zoologica 50:1–39.Google Scholar
  11. Brower, L.P., Brower, J.V.Z., andCorvino, J.M. 1967. Plant poisons in a terrestrial food chain.Proc. Natl. Acad. Sci. 57:892–898.Google Scholar
  12. 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
  13. 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
  14. 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
  15. Brown, F.M. andHeineman, B. 1972. Jamaica and its Butterflies. E.W. Classey, Ltd., London.Google Scholar
  16. Brown, K.S. 1984. Adult-obtained pyrrolizidine alkaloids defend ithomiine butterflies against a spider predator.Nature 309:707–709.Google Scholar
  17. Bull, L.B., Culvenor, C.C.J., andDick, A.T. 1968. The Pyrrolizidine Alkaloids. North-Holland Publishing Co., Amsterdam.Google Scholar
  18. Chermock, R.L. 1947. A new subspecies ofLimenitis archippus (Lepidoptera, Nymphalidae).Am. Mus. Novit. 1365:1–2.Google Scholar
  19. Cohen, J.A. 1983. Chemical interaction among milkweed plants (Asclepiadaceae) and lepidopteran herbivores. PhD dissertation. University of Florida, Gainesville.Google Scholar
  20. Cohen, J.A. 1985. Differences and similarities in cardenolide content of queen and monarch butterflies in Florida and their ecological and evolutionary implications.J. Chem. Ecol. 11:85–103.Google Scholar
  21. Conner, W.E., Eisner, T., Van der Meer, R.K., Guerrero, A., andMeinwald, J. 1981. Precopulatory sexual interaction in an arctiid moth (Utetheisa ornatrix): Role of a pheromone derived from dietary alkaloids.Behav. Ecol. Sociobiol. 9:227–235.Google Scholar
  22. Coppinger, R.P. 1970. The effect of experience and novelty on avian feeding behavior with reference to the evolution of warning coloration in butterflies. II. Reactions of naive birds to novel insects.Am. Nat. 104:323–335.Google Scholar
  23. Edgar, J.A., Boppré, M., andSchneider, D. 1979. Pyrrolizidine alkaloid storage in African and Australian danaid butterflies.Experientia 35:1447–1448.Google Scholar
  24. Eisner, T. 1980. Chemistry, defence and survival: case studies and selected topics, pp. 847–878,in M. Locke and D.S. Smith (eds.). Insect Biology in the Future. Academic Press, New York.Google Scholar
  25. Glendinning, J.I.,Brower, L.P., andMontgomery, C.A. 1990. Taste and toxic responses of three mice species to cardiac glycosides and pyrrolizidine alkaloids.Chemoecology. In press.Google Scholar
  26. Hegnauer, R. 1964.Chemotaxonomie der Pflanzen. Band 3. Birkhauser e Verlag, Basel.Google Scholar
  27. Holm, R.W. 1950. The American species ofSarcostemma R. Br. (Asclepiadaceae).Ann. Mo. Bot. Garden 37:477–560.Google Scholar
  28. Malcolm, S.B. 1990. Mimicry: Status of a classic evolutionary paradigm.Trends Ecot. Evol. 5:57–62.Google Scholar
  29. Malcolm, S.B., Cockrell, B.J., andBrower, L.P. 1989. Cardenolide fingerprint of monarch butterflies reared on common milkweed,Asclepias syriaca L.J. Chem. Ecol. 15:819–853.Google Scholar
  30. Malcolm, S.B.,Cockrell, B.J., andBrower, L.P. 1991. Spring migration of the monarch butterfly: cardenolide content and wing wear as labels of successive brood migration,in S.B. Malcolm and M.P. Zalucki (eds.). Biology and Conservation of the Monarch Butterfly. Natural History Museum of Los Angeles County, Contributions in Science. In press.Google Scholar
  31. Masters, A.R. 1990. Pyrrolizidine alkaloids in artificial nectar protect adult ithomiine butterflies from a spider predator.Biotropica 22:298–304.Google Scholar
  32. 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. 7:981–1009.Google Scholar
  33. Nishio, S. 1980. The fates and adaptive significance of cardenolides sequestered by larvae ofDanaus plexippus (L.) andCycnia inopinatus (Hy. Edwards). PhD dissertation. University of Georgia, Athens.Google Scholar
  34. Opler, P.A., andKrizek, G.O. 1984. Butterflies East of the Great Plains. Johns Hopkins University Press, Baltimore.Google Scholar
  35. Parsons, J.A. 1965. A digitalis-like toxin in the monarch butterfly,Danaus plexippus.J. Physiol. 178:290–304.PubMedGoogle Scholar
  36. Pliske, T.E. 1975. Attraction of Lepidoptera to plants containing pyrrolizidine alkaloids.Environ. Entom. 4:455–473.Google Scholar
  37. Pliske, T.E., andEisner, T. 1969. Sex pheromone of the queen butterfly: biology.Science 164:1170–1172.Google Scholar
  38. Reichstein, T., Euw, J. Von, Parsons, J.A., andRothschild, M. 1968. Heart poisons in the monarch butterfly.Science 161:861–866.PubMedGoogle Scholar
  39. Ritland, D.B. 1991a. Revising a classic butterfly mimicry scenario: Demonstration of Müllerian mimicry between Florida viceroys (Limenitis archippus floridensis) and queens (Danaus gilippus berenice).Evolution. In press.Google Scholar
  40. Ritland, D.B. 1991b. Unpalatability of the viceroy butterfly (Limenitis archippus) and its purported mimicry model, the Florida queen (Danaus gilippus).Oecologia. In press.Google Scholar
  41. Ritland, D.B. 1991c. Reassessment of viceroy butterfly (Limenitis archippus) mimicry and an analysis of the ecological dynamics of mimicry. PhD dissertation. University of Florida, Gainesville.Google Scholar
  42. Ritland, D.B., andBrower, L.P. 1991. The viceroy butterfly is not a Batesian mimic.Nature 350:497–498.Google Scholar
  43. 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.)).Recent Adv. Phytochem. 10:93–167.Google Scholar
  44. Rosatti, T.J. 1989. The genera of suborder Apocynineae (Apocynaceae and Asclepiadaceae) in the southeastern United States.J. Arnold Arbor. 70:443–514.Google Scholar
  45. Rothschild, M. 1972. Secondary plant substances and warning colouration in insects, pp. 59–83,in H.F. van Emden (ed.). Insect/Plant Relationships. Blackwell Scientific Publishers, Oxford, U.K.Google Scholar
  46. Rothschild, M., andMarsh, N.A. 1978. Some peculiar aspects of danaid/plant relationships.Entomol. Exp. Appl. 24:437–450.Google Scholar
  47. Rothschild, M., Euw, J. Von, Reichstein, T., Smith, D.A.S., andPierre, J. 1975. Cardenolide storage inDanaus chrysippus with additional notes onD. plexippus.Proc. R. Soc. (B) 190:1–31.Google Scholar
  48. Schlee, M.A. 1986. Avian predation on Heteroptera: experiments on the European blackbirdTurdus m. merula L.Ethology 73:1–18.Google Scholar
  49. Scudder, S.H. 1870. Is mimicry advantageous?Nature 3:147.Google Scholar
  50. Wratten, S.D., Edwards, P.J., andWinder, L. 1988. Insect herbivory in relation to dynamic changes in host plant quality.Biol. J. Linn. Soc. 35:339–350.Google Scholar

Copyright information

© Plenum Publishing Corporation 1991

Authors and Affiliations

  • David B. Ritland
    • 1
  1. 1.Department of ZoologyUniversity of FloridaGainesville

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