Skip to main content
Log in

Responses of three mouse species to deterrent chemicals in the monarch butterfly. I. Taste and toxicity tests using artificial diets laced with digitoxin or monocrotaline

  • Research papers
  • Published:
CHEMOECOLOGY Aims and scope Submit manuscript

Summary

Of three common mouse species at the Mexican overwintering sites of the monarch butterfly, onlyPeromyscus melanotis eats monarchs. We hypothesized thatP. aztecus andReithrodontomys sumichrasti reject monarchs because they are more sensitive to the bitter taste and/or toxic effects of the cardiac glycosides (CGs) and pyrrolizidine alkaloids (PAs) in the butterflies. Two-choice preference tests revealed no difference in taste avoidance thresholds to free base and N-oxide forms of the PA, monocrotaline, but very different avoidance thresholds to the CG, digitoxin. Avoidance thresholds forR. sumichrasti andP. aztecus were, in respective order, 1020 and 34 times less than that forP. melanotis. We also tested the toxic sensitivity of juvenile mice by chronically feeding diets containing digitoxin or monocrotaline at concentrations similar to those used in the preference tests. No species developed CG toxicity, but bothP. melanotis andP. aztecus developed moderate PA toxicity (R. sumichrasti was not tested for PA toxicity).P. aztecus grew more slowly and manyP. melanotis had hepatic metabolic lesions. Thus, the three mouse species responded very differently to the taste and toxic properties of CGs and PAs at ecologically relevant concentrations: 1) CGs were taste rejected by all species exceptP. melanotis, while PAs were not; and 2) PAs were toxic, while CGs were not.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barnes CD, Eltherington LG (1973) Drug Dosages in Laboratory Animals: a Handbook. Berkeley, California: University of California Press

    Google Scholar 

  • Baron RL (1980) Chronic studies. Pp 191–210in Galli CL, Murphy SD, Paolletti R (eds) The Principles and Methods in Modern Toxicology. Elsevier/North-Holland Biomedical Press

  • Bate-Smith EC (1972) Attractants and repellents in higher animals. Pp 45–56in Harborne JB (ed) Phytochemical Ecology: Proceedings of the Phytochemical Society Symposium. London: Academic Press

    Google Scholar 

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

    Google Scholar 

  • Brower LP (1984) Chemical defense in butterflies. Pp 109–134in Vane-Wright RI, Ackery PR (eds) The Biology of Butterflies. London: Academic Press

    Google Scholar 

  • Brower LP (1985) New perspectives on the migration biology of the monarch butterfly,Danaus plexippus L. Univ Texas Marine Sci Inst, Contrib Marine Sci 27 (Suppl):748–785

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

    Google Scholar 

  • Brower LP, Nelson CJ, Fink LS, Seiber JN, 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 447–476in Spencer KC (ed) Chemical Mediation of Coevolution. New York: Academic Press

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Calvert WH, Brower LP (1986) The location of monarch butterfly (Danaus plexippus L.) overwintering colonies in Mexico in relation to topography and climate. J Lepid Soc 40:164–187

    Google Scholar 

  • Carpenter JA (1956) Species differences in taste preference. J Comp & Physiol Psychol 49:139–144

    Google Scholar 

  • Chrzanowski Z (1965) Die Auswahlschwelle, die Abweisschwelle und die Geschmackstoleranz von Wasserlösungen des Chininhydrochlorids, der Zitronensäure, der Sacharose und des Kochsalzes einiger Arten von Insektenfressern und Nagetieren. Acta Biol Exp 25:37–58

    Google Scholar 

  • Craig JC, Purushothaman KK (1970) An improved preparation of tertiary amine N-oxides. J Org Chem 35:1721–1722

    PubMed  Google Scholar 

  • Detweiler DK (1967) Comparative pharmacology of cardiac gylcosides. Feder Proceed 26:1119–1124

    Google Scholar 

  • Edgar JA, Cockrum PA, Frahn JL (1976) Pyrrolizidine alkaloids inDanaus plexippus L. andDanaus chrysippus L. Experientia 32:1535–1536

    Google Scholar 

  • Eisner T (1980) Chemistry, defense, and survival: case studies and selected topics. Pp 847–878in Locke M, Smith DS (eds) Insect Biology in the Future. New York: Academic Press

    Google Scholar 

  • Galef BG (1987) Social influences on the identification of toxic foods by Norway rats. Anim Learn & Behav 15:327–332

    Google Scholar 

  • Ganchrow JR (1977) Consummatory responses to taste stimuli in the hedgehog(Erinaceus europaeus). Physiol & Behav 18:447–453

    Google Scholar 

  • Garcia J, Hankins WG, Rusiniak KW (1974) Behavioral regulation of the milieu interne in man and rat. Science 185:824–831

    PubMed  Google Scholar 

  • Garcia J, Hankins WG (1975) The evolution of bitter and the acquisition of toxiphobia. Pp 39–45in Denton DA, Coghlan JP (eds) Olfaction and Taste V. Proceedings of the 5th International Symposium in Melbourne, Australia. New York: Academic Press

    Google Scholar 

  • Gardner RJ (1978) Lipophilicity and bitter taste. J Pharm Pharmac 30:531–532

    Google Scholar 

  • Gardner RJ (1979) Lipophilicity and the perception of bitterness. Chem Senses and Flav 4:275–286

    Google Scholar 

  • Gescheider GA (1976) Psychophysics: method and theory. Hillsdale, New Jersey: Lawrence Erlbaum Associates, Publishers

    Google Scholar 

  • Glendinning JI (1989) Comparative responses of five sympatric species of mice to overwintering colonies of monarch butterflies in Mexico. PhD Dissertation. Gainesville, Florida: University of Florida

    Google Scholar 

  • Glendinning JI (1990) Responses of three mouse species to deterrent chemicals in the monarch butterfly. II. Tests using intact monarchs. Chemoecology 1:124–130

    Google Scholar 

  • Glendinning JI (1991) Comparative feeding responses of the micePeromyscus melanotis, P. aztecus, Reithrodontomys sumichrasti, andMicrotus mexicanus 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, Brower LP (1991) Feeding and breeding responses of five mice species to overwintering aggregations of the monarch butterfly. J Anim Ecol 59:1091–1112

    Google Scholar 

  • Goeger DE, Cheeke PR, Ramsdell HS, Nicholson SS, Buhler DR (1983) Comparison of the toxicities ofSenecio jacobea, Senecio vulgaris andSenecio glabellus in rats. Toxicol Lett 15:19–23

    PubMed  Google Scholar 

  • Gould SJ, Vrba ES (1982) Exaptation — a missing term in the science of form. Paleobiol 8:4–15

    Google Scholar 

  • Harder DB, Maggio JC, Whitney G (1989) Assessing gustatory detection capabilities using preference procedures. Chem Senses 14:547–564

    Google Scholar 

  • Jacobs WW, Beauchamp GK, Kare MR (1978) Progress in animal flavor research. Pp 1–20in Bullard RW (ed) Flavor Chemistry of Animal Foods. Washington, DC: American Chemical Society

    Google Scholar 

  • Janzen DH, Fellows LE, Waterman PG (1990) What protectsLonchocarpus (Leguminosae) seeds in a Costa Rican dry forest? Biotropica 22:272–285

    Google Scholar 

  • Jones TC, Hunt RD (1983) Veterinary pathology, fifth edition. Philadelphia: Lea & Febiger

    Google Scholar 

  • Kelley RB, Seiber JN, Jones HJ, Segall HJ, Brower LP (1987) Pyrrolizidine alkaloids in overwintering monarch butterflies.(Danaus plexippus) from Mexico. Experientia 43:943–946

    Google Scholar 

  • Malcolm SB, Brower LP (1989) Evolutionary and ecological implications of cardenolide sequestration in the monarch butterfly. Experientia 45:284–294

    Google Scholar 

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

    Google Scholar 

  • Marty MM (1983) Disposition and metabolism of milkweed (Asclepiadaceae) cardenolides in monarch butterfly larvae,Danaus plexippus, and in a predator,Peromyscus maniculatus. PhD Dissertation. University of California, Davis

    Google Scholar 

  • Mattocks AR (1971) Hepatotoxic effects due to pyrrolizidine alkaloid Noxides. Xenobiot 1:563–565

    Google Scholar 

  • Mattocks AR (1986) Chemistry and Toxicology of Pyrrolizidine Alkaloids. New York: Academic Press

    Google Scholar 

  • McLean E, Bras G, György P (1964) Veno-occlusive lesions in livers of rats fedCrotalaria fulva. Brit J Exp Pathol 45:242–247

    Google Scholar 

  • Patton HD, Ruch TC (1944) Preference thresholds for quinine hydrochloride in chimpanzee, monkey and rat. J Comp Psychol 37:35–49

    Google Scholar 

  • Peterson JE, Jago MV, Reddy JK, Jarrett RG (1983) Neoplasia and chronic disease associated with prolonged administration of dehydroheliotridine to rats. J Natl Cancer Inst 70:381–386

    PubMed  Google Scholar 

  • Pressman TG, Doolittle JH (1966) Taste preferences in the Virginia opossum. Psychol Rep 18:875–878

    Google Scholar 

  • Provenza FD, Balph DF, Olsen JD, Dwyer DD, Ralphs MH, Pfister MH (1988) Toward understanding behavioral responses of livestrock to poisonous plants. Pp 407–424in James LF, Ralphs MH, Nielson DB (eds) The Ecology and Economic Impact of Poisonous Plants on Livestock Production. Boulder, Colorado: Westview Press

    Google Scholar 

  • Ralphs MH, Olsen JD (1987) Alkaloids and palatability of poisonous plants. Pp 78–83in Provenza FD, Flinders JT, McAurthur ED (eds) Alkaloids and Palatability of Poisonous Plants. Ogden, Utah: Intermountain Research Station, Forest Service, U.S. Department of Agriculture

    Google Scholar 

  • Robbins SL, Cotran RS (1979) Pathologic Basis of Disease. 2nd edition. Philadelphia: WB Saunders Co

    Google Scholar 

  • Rogers JG Jr (1974) Responses of caged red-winged blackbirds to two types of repellents. J Wildl Manage 38:418–423

    Google Scholar 

  • Rothschild M, Marsh N (1978) Some peculiar aspects of Danaid/plant relationships. Ent Exp & Appl 24:437–450

    Google Scholar 

  • Rozin P (1969) Adaptive food sampling patterns in vitamin deficient rats. J Comp Physiol Psych 69:126–132

    Google Scholar 

  • Rzóska J (1953) Bait shyness, a study in rat behavior. Anim Behav 1:128–135

    Google Scholar 

  • Schoental R, Magee PN (1957) Chronic liver changes in rats after a single dose of lasiocarpine, a pyrrolizidine(Senecio) alkaloid. J Path Bact 74:305–319

    Google Scholar 

  • Schwartz NN, Blumbergs JH (1964) Epoxidations with m-chloroperbenzoic acid. J Org Chem 29:1976–1978

    Google Scholar 

  • Scott TR, Mark GP (1987) The taste system encodes stimulus toxicity. Brain Res 414:197–203

    PubMed  Google Scholar 

  • Seiber JN, Brower LP, Lee SM, McChesney MM, Cheung HTA, Nelson C, Watson TR (1986) Cardenolide connection between overwintering monarch butterflies from Mexico and their larval food plant,Asclepias syriaca. J Chem Ecol 12:1157–1170

    Google Scholar 

  • Smith JC, Williams DP, Short Jue S (1976) Rapid oral mixing of glucose and saccharin by rats. Science 191:304–305

    PubMed  Google Scholar 

  • Tanz RD, Urquilla PR (1982) Cardiac glycosides. Pp 269–281in Craig CR, Stitzel RE (eds) Modern Pharmacology. Boston: Little, Brown & Company

    Google Scholar 

  • Valenstein ES, Cox VC, Kakolewski JW (1967) Polydipsia elicited by the synergistic action of a saccharin and glucose solution. Science 157:552–554

    PubMed  Google Scholar 

  • Vaughan TA, Czaplewski NJ (1985) Reproduction in Stephen's woodrat: the wages of folivory. J Mamm 66:429–443

    Google Scholar 

  • Warren RP, Pfaffman C (1959) Early experience and taste aversion. J Comp Physiol Psychol 52:63–66

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Glendinning, J.I., Brower, L.P. & Montgomery, C.A. Responses of three mouse species to deterrent chemicals in the monarch butterfly. I. Taste and toxicity tests using artificial diets laced with digitoxin or monocrotaline. Chemoecology 1, 114–123 (1990). https://doi.org/10.1007/BF01241652

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01241652

Key words

Navigation