Lincoln P. Brower

Ecological Chemistry and the Palatability Spectrum

A new bioassay for comparing the palatability to avian predators of monarch butterflies reared on various asclepiadaceous food plants containing cardiac glycosides indicates a palatability spectrum. The monarchs reared on one plant species are six times as emetic as those fed another, while those raised on an asclepiad which lacks cardiac glycosides are not emetic at all.

Localization of Heart Poisons in the Monarch Butterfly

The cardiac glycosides that monarch butterflies sequester from milkweed plants during the larval stage differ remarkably in their emetic potency and are concentrated to different degrees in the various parts of the body as well as in the two sexes (Fig. 1). The very high concentrations of these compounds in the wings probably facilitate learned taste rejection in predators and account for the relatively high frequency of Danaid butterflies with beak-marked wings in natural populations. The cardiac glycosides in the abdomen have a much higher emetic potency than those in the rest of the body. Consequently, naive, extremely hungry, or forgetful birds which capture and peck off the wings but eat the abdomen discard the least emetic glycosides and ingest the most emetic, and thus again experience emesis. The nonrandom distribution of cardenolides in the wings, abdomen, and thorax, together with the fact that monarch males not only contain lower concentrations of cardiac glycosides than females but also contain cardenolides that are overall less emetic than those in females, is interpreted as evidence that these poisons are incorporated at a physiological cost. This cost, balanced against the benefits of protection from predation, provides a selective basis for the occurrence of both emetic and nonemetic individuals in natural populations. Since birds can discriminate emetic from nonemetic monarchs on the basis of taste, it is not necessary to invoke theories of kind of group selection to explain the evolution of this kind of unpalatability.

Variation in cardiac glycoside content of monarch butterflies from natural populations in eastern North America.

A new spectrophotometric assay has been used to determine the gross concentration of cardiac glycoside in individual monarch butterflies. Adults sampled during the fall migration in four areas of eastern North America exhibited a wide variation in cardiac glycoside concentration. The correlation between spectrophotometrically measured concentrations and emetic dose determinations supports the existence of a broad palatability spectrum in wild monarch butterflies. The cardiac gylcoside concentration is greater in females than in males and is independent of the dry weight of the butterflies; contrary to prediction, both the concentration mean and variance decrease southward. The defensive advantage of incorporating cardiac glycosides may be balanced by detrimental effects on individual viability.

Mortality of the Monarch Butterfly (Danaus plexippus L.): Avian Predation at Five Overwintering Sites in Mexico

Analyses of predated butterflies on the forest floor at five monarch overwintering sites in Mexico and observations of birds foraging in mixed flocks indicate that individual birds of several species have learned to penetrate the monarchs cardenolide-based chemical defense. Predation is inversely proportional to colony size and appears to be one evolutionary explanation of the dense aggregations.

Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies

1. Monarch butterflies Danaus plexippus (L.) (Lepidoptera: Nymphalidae) are susceptible to infection by the obligate protozoan parasite Ophryocystis elektroscirrha (McLaughlin and Myers) (Apicomplexa: Neogregarinida). Because monarchs form resident and migratory populations in different parts of the world, this host–parasite system provides the opportunity to examine how variation in parasite prevalence relates to host movement patterns.

Milkweed Cardenolides and Their Comparative Processing by Monarch Butterflies (Danaus plexippus L.)

The milkweed family (Asclepiadaceae) comprises some 200 genera and 2500 species of perennial shrubs, herbs and vines distributed throughout the tropics and extending to temperate areas of the world. They include some highly prized ornamentals and economically significant weeds, and are generally characterized to the layman by the milky latex they exude when a leaf or other organ is ruptured. Chemical interest in the milkweeds has been stimulated by the use of some plants in medicinal preparations to treat cancers, tumors, and warts (Refs. in 54), as emetics, to treat bronchitis (Refs. in 64), and as a source of digitalislike therapeutic agents (Refs. in 44). They are also known for their poisonous nature, which has found advantageous use in the preparation of arrow poisons, and also causes occasional but extensive poisoning episodes among grazing sheep and cattle in milkweed-infested rangelands52,58.

Experimental Studies of Mimicry. 5. The Reactions of Toads (Bufo terrestris) to Bumblebees (Bombus americanorum) and Their Robberfly Mimics (Mallophora bomboides), with a Discussion of Aggressive Mimicry

1. Laboratory experiments described in this paper support the hypothesis of Batesian mimicry of bumblebees (Bombus americanorum) by asilid flies (Mallophora bomboides). Seven Southern toads (Bufo terrestris) were used as caged predators. 2. Experimental toads which initially attacked bumblebees learned to reject them on sight alone. They then also rejected mimics to a significantly greater extent than control toads which did not have prior experience with the bumblebees. 3. Two of the three control toads also freely are bumblebees from which the sting had been removed. This indicates that the noxious quality is the sting. 4. Field observations of the predatory behavior of the adult flies in south central Florida show that the mimetic flies prey extensively upon their bumblebee models. 5. The idea of aggressive mimicry, proposed but then discarded by Poulton, is reconsidered in the light of new evidence and it is concluded that the selective basis for the resemblance of bees by flies, in addition to being Batesian mimicry, may in part also be the visual selection resulting from the defensive behavior of the models towards the mimics which attack them.

Evolutionary and ecological implications of cardenolide sequestration in the monarch butterfly

Monarch butterflies sequester cardenolides from their larval host plants in the milkweed genusAsclepias for use in defense against predation. Of 108Asclepias species in North America, monarchs are known to feed as larvae on 27. Research on 11 of these has shown that monarchs sequester cardenolides most effectively, to an asymptote of approximately 350 μg/0.1 g dry butterfly, from plants with intermediate cardenolide contents rather than from those with very high or very low cardenolide contents. SinceAsclepias host plant species are distributed widely in space and time across the continent, monarchs exploit them by migration between breeding and overwintering areas. After overwintering in central Mexico, spring migrants east of the Rocky Mountains exploit three predominantAsclepias species in the southern USA that have moderately high cardenolide contents. Monarchs sequester cardenolides very effectively from these species. First generation butterflies are thus well protected against predators and continue the migration north. Across the northern USA and southern Canada most summer breeding occurs on a fourthAsclepias species and in autumn most of these monarchs migrate back to Mexican overwintering sites. The ecological implications of this cycle of cardenolide sequestration for the evolution of monarch migration are discussed.

Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata

1. A novel experimental method was developed to study negative physical and chemical effects of latex and cardiac glycosides on first‐instar monarch butterfly larvae in their natural environment in north central Florida. Forceps were used to nibble through the petioles of leaves of the sandhill milkweed Asclepias humistrata, mimicking the behaviour of mature monarch larvae. This notching cut off the supply of latex to the leaves without significantly reducing either their cardiac glycoside concentration or water content.

Plant-determined variation in the cardenolide content, thin-layer chromatography profiles, and emetic potency of monarch butterflies,Danaus plexippus reared on the milkweed,Asclepias eriocarpa in California.

This paper is the first in a series on cardenolide fingerprinting of the monarch butterfly. New methodologies are presented which allow both qualitative and quantitative descriptions of the constituent cardenolides which these insects derive in the wild from specificAsclepias foodplants. Analyses of thin-layer Chromatographic profiles ofAsclepias eriocarpa cardenolides in 85 individual plant-butterfly pairs collected at six widely separate localities in California indicate a relatively invariant pattern of 16–20 distinct cardenolides which we here define as theAsclepias eriocarpa cardenolide fingerprint profile. Cardenolide concentrations vary widely in the plant samples, but monarchs appear able to regulate total storage by increasing their concentrations relative to their larval host plant when reared on plants containing low concentrations, and vice versa. Forced-feeding of blue jays with powdered butterfly and plant material and with one of the constituent plant cardenolides, labriformin, established that theA. eriocarpa cardenolides are extremely emetic, and that monarchs which have fed on this plant contain an average of 16 emetic-dose fifty (ED50) units. The relatively nonpolar labriformin and labriformidin in the plant are not stored by the monarch but are metabolized in vivo to desglucosyrioside which the butterfly does store. This is chemically analogous to the way in which monarchs and grasshoppers metabolize another series of milkweed cardenolides, those found inA. curassavica. It appears that the sugar moiety through functionality at C-3′ determines which cardenolides are metabolized and which are stored. The monarch also appears able to store several lowRf cardenolides fromA. eriocarpa without altering them. Differences in the sequestering process in monarchs and milkweed bugs (Oncopeltus) may be less than emphasized in the literature. The monarch is seen as a central organism involved in a coevolutionary triad simultaneously affecting and affected by both its avian predators and the secondary chemistry of the milkweeds with which it is intimately involved.