Responses of three mouse species to deterrent chemicals in the monarch butterfly. II. Taste tests using intact monarchs

Summary Peromyscus melanotis is the only one of three mouse species that eats monarch butterflies at their overwintering sites in Mexico. I tested two hypotheses: 1)P. aztecus avoids monarchs because of a bitter taste aversion to cardiac glycosides (CGs) and an inability to reject CG-rich body parts; 2)Reithrodontomys sumichrasti avoids monarchs principally because of a bitter taste aversion to the CGs. None of the species are sensitive to the toxic effects of ingested CGs. Feeding responses of laboratory-reared mice of each species to monarchs with low, medium and high CG concentrations were compared. BothP. aztecus andR. sumichrasti ate significantly fewer of all three types of monarchs thanP. melanotis. ForP. aztecus andR. sumichrasti, the number of monarchs eaten decreased with increasing CG concentration, whereas forP. melanotis, the number remained constant.Peromyscus melanotis andR. sumichrasti developed a feeding technique for rejecting the CG-laden cuticular material, which reduced the bitterness of ingested monarch material. However,R. sumichrasti displayed the technique significantly less often thanP. melanotis; andP. aztecus never developed it. I conclude that high taste sensitivity to CGs and less versatile food handling preventP. aztecus andR. sumichrasti from overcoming the monarch's chemical defenses.     

Milkweeds,monarch butterflies and the ecological significance of cardenolides

Summary The contribution of Miriam Rothschild to the monarch cardenolide story is reviewed in the light of the 1914 challenge by the evolutionary biologist, E.B. Poulton for North American chemists to explain the chemical basis of unpalatability in monarch butterflies and their milkweed host plants. This challenge had lain unaccepted for nearly 50 years until Miriam Rothschild took up the gauntlet and showed with the help of many able colleagues that monarchs are aposematically coloured because they sequester toxic cardenolides from milkweed host plants for use as a defence against predators. By virtue of Dr Rothschild's inspiration and industry, and subsequently that of Lincoln Brower and his colleagues, this tritrophic interaction has become a familiar paradigm for the evolution of chemical defences and warning colouration. We now know that the cardenolide contents of different milkweeds vary quantitatively, qualitatively and spatially, both within and among species and we are starting to appreciate the implications of such variation. However, as Dr Rothschild has pointed out in her publications, cardenolides have sometimes blinded us to reality and it is curious how little evidence there is for a defensive function to cardenolides in plants — especially against adapted specialists such as the monarch. Thus the review will conclude with a discussion of the significance of temporal variation and induction of cardenolide production in plants, the lethal plant defence paradox and an emphasis on the dynamics of the cardenolide-mediated interaction between milkweeds and monarch larvae.     

Chemical defence in chewing and sucking insect herbivores: Plant-derived cardenolides in the monarch butterfly and oleander aphid

Summary Cardenolide sequestration by a hemimetabolous aphid and a holometabolous butterfly from the neotropical milkweed,Asclepias curassavica L., is compared. The oleander aphid,Aphis nerii B. de F., sequestered a similarly narrow range of cardenolide concentrations to the monarch butterfly,Danaus plexippus (L.), from the wide range of concentrations available in leaves of A.curassavica. However, A.nerii sequestered significantly less cardenolide (269 µg/0.1 g) thanD. plexippus (528 µg/0.1 g). The honeydew excreted by A.nerii was comprised of 46% cardenolide. The complete polarity range of 25 cardenolides detected by thin layer chromatography in A.curassavica was represented in the 17 whole aphid cardenolides and the 20 aphid honeydew cardenolides detected. D.plexippus sequestered a narrower polarity range of 11 cardenolides, having eliminated low polarity cardenolide genins and glycosides. It is suggested that these chemical differences may be related to interactions among the broad feeding tactics of sucking or chewing milkweed leaves, life history constraints of holometabolyversus hemimetaboly, the distribution of milkweed food resources in space and time, and the dynamics of natural enemies.