Abstract
Seven analogs of aristolochic acids (I, II, III, B, C, D, and E) were isolated from the leaves ofAristolochia debilis and characterized as the larval feeding stimulants of an Aristolochiaceae-feeding swallowtail butterfly,Atrophaneura alcinous. Aristolochic acids showed synergistic activity in combination with the water-soluble components in the leaf extract. Aristolochic acids were detected in the body tissues and specialized organs throughout all life stages ofA. alcinous. Larval osmeterial fluid contained aristolochic acids as high as 2% of the secretions, the compositions of which were similar to that found in the leaf extracts. In contrast, the eggs selectively contained aristolochic acids I and II. These two acids were present both in the egg yolk and egg coating material as well as in the collateral glands (glandulae sebaceae) of the adult females. The cannibalistic activity of the larvae against the eggs and pupae seemed to be triggered by aristolochic acids present on the egg surface and pupal cuticle, suggesting a possible adaptive mechanism in this species. Aristolocic acid I deterred feeding of tree sparrows, which suggested a defensive role against vertebrate predators.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Brower, L.P. 1961. Experimental analysis of egg cannibalism in the monarch and queen butterflies,Danaus plexippus andD. gilippus berenice.Physiol. Zool. 34:287–296.
Brower, L.P. 1984. Chemical defense in butterflies, pp. 109–134,in R.I. Vane-Wright and P.R. Ackery (eds.). The Biology of Butterflies. Academic Press, New York.
Brown, K.S., Jr., Damman A.J., andFeeny, P. 1980. Troidine swallowtails (Lepidoptera, Papilionidae) in southeastern Brazil: Natural history and foodplant relationships.J. Res. Lepid. 19:199–226.
Chen, Z.H., Huang, B.S., Zhu, D.Y., andYin, M.L. 1981. Studies on the active principles ofAristolochia debilis. II. 7-Hydroxyaristolochic acid-A and 7-methoxyaristolochic acid-A.Hua Hsueh Hsueh Pao 39:239–242.
David, W.A.L., andGardiner, B.O.C. 1962. Oviposition and the hatching of the eggs ofPieris brassicae (L.) in a laboratory culture.Bull. Entomol. Res. 53:91–109.
Euw, J.v., Reichstein, T., andRothschild, M. 1968. Aristolochic acid-I in the swallowtail butterflyPachliopta aristolochiae Fabr. (Papilionidae).Isr. J. Chem. 6:659–670.
Honda, K. 1980a. Odor of a papilionid butterfly. Odoriferous substances emitted byAtrophaneura alcinous alcinous (Lepidoptera: Papilionidae).J. Chem. Ecol. 5:867–873.
Honda, K. 1980b. Osmeterial secretions of papilionid larvae in the generaLeudorfia, Graphium and Atrophaneura (Lepidoptera).Insect Biochem. 10:583–588.
Kupchan, S.M., andMerianos, J.J. 1968. The isolation and structural elucidation of novel derivatives of aristolochic acid fromAristolochia indica.J. Org. Chem. 33:3735–3738.
Kupchan, S.M., andWormser, H.C. 1965. Tumor inhibitors. X. Photochemical synthesis of phenanthrenes. Synthesis of aristolochic acid and related compounds.J. Org. Chem., 30:3792–3800.
Kupchan, S.M., Wormser, H.C., andSasso, M. 1965. Tumor inhibitors. XI. Proof of structure of aristolochic acid-C by total synthesis of its methyl ester methyl ester.J. Org. Chem. 30:3935–3937.
Miller, J., andFeeny, P. 1983. Effects of benzylisoquinoline alkaloids on the larvae of polyphagous Lepidoptera.Oecologia 58:332–339.
Mix, D.B., Guinaudeau, H., andShamma, M. 1983. The aristolochic acids and aristolactams.J. Nat. Prod. 45:657–666.
Moretti, C., Rideau, M., Chenieux J.C., andViel, C. 1979. Isolation of aristolochic acid from two Madagascar Aristolochiaceae. Determination of its toxicity on vegetal cells. Comparison with animal cells.Planta Med. 35:360–365.
Nishida, R., andFukami, H. 1989. Ecological adaptation of an Aristolochiaceae-feeding swallowtail butterfly,Atrophaneum alcinous, to aristolocic acids.J. Chem. Ecol. 15:2565–2575.
Nishida, R., Tan, K.H., Serit, M., Lajis, N.H., Sukari, A.M., Takahashi, S., andFukami, H. 1988. Accumulation of phenylpropanoids in the rectal glands of male Oriental fruit fly. Dacus dorsalis.Experientia 44:534–536.
Pailer, M., andBergthaller, P. 1966. Pflanzliche Naturstoffe mit einer Nitrogruppe. 5. Die Konstitution der Arisolochiasäuren III und IIIa.Monatsch. Chem. 97:484–493.
Pailer, M., andSchleppnik, A. 1957. Pflanzliche Naturstoffe mit einer Nitrogruppe. II. Die Konstitution der Aristolochiasäure II.Monatsh. Chem. 88:367–387.
Pailer, M., Belohlav, L., andSimonitsch, E. 1956. Pflanzliche Naturstoffe mit einer Nitrogruppe. I. Die Konstitution der Aristolochias↑re.Monatsh. Chem. 87:249–268.
Pailer, M., Bergthaller, P., andSchaden, G. 1965. Pflanzliche Naturstoffe mit einer Nitrogruppe. 4. Über die Isolierung und Characterisierung von vier neuen Aristolochiasäuren (ausAristolochia dematitis L.).Monatsh. Chem. 96:863–883.
Rothschild, M., Euw, J.v., andReichstein, T. 1972. Aristolochic acids stored byZerynthia polyxena (Lepidoptera).Insect Biochem. 2:334–343.
Sasagawa, S. 1962. Studies on the ingredients of aristolochiaceous plants. IV. Aristolochic acid derivatives and acid C derivatives.Yakugaku Zasshi 82:921–925.
Tomita, M., andKura, S. 1957. Studies on the ingredients of aristolochiaceous plants. I. The ingredients ofAristolochia kampferi Willd andA. debilis Sieb, et Zucc.Yakugaku Zasshi 77:812–814.
Tomita, M., andKura, S. 1959. Studies on the ingredients of aristolochiaceous plants. II. The ingredients of Chinese drug “Fang-chi” (2).Yakugaku Zasshi 79:973–976.
Tomita, M., andSasagawa, S. 1959. Studies on the ingredients of aristolochiaceous plants. III. The ingredients ofAristolochia debilis Sieb, et Zucc. and of the Chinese drug “Fang-chi” in Formosa.Yakugaku Zasshi 79:1470–1479.
Urzúa, A., andPriestap, H. 1985. Aristolochic acids fromBattus polydamas Biochem.Syst. Ecol. 13:169–170.
Urzúa, A., Salgado, G., Gassels, B.K., andEckhardt, G. 1983. Aristolochic acids inAristolochia chilensis and theAristolochia-feeder, Battus archidamas (Lepidoptera).Collect. Czech. Chem. Commun. 48:1513–1519.
Verschaffelt, E. 1911. The cause determining the selection of food in some herbivorous insects.Proc. K. Ned. Akad. Wet. 13:536–542.
Williams, K.S., andGillbert, L.E. 1981. Insects as selective morphology: Egg mimicry reduces egg laying by butterflies.Science 212:467–469.
Young, A.M. 1977. Studies on the biology ofParides iphidamas in Costa Rica.J. Lepid. Soc. 31:100–108.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Nishida, R., Fukami, H. Ecological adaptation of an Aristolochiaceae-feeding swallowtail butterfly,Atrophaneura alcinous, to aristolochic acids. J Chem Ecol 15, 2549–2563 (1989). https://doi.org/10.1007/BF01014731
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01014731