Stephen B. Malcolm

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.

Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox

All terrestrial vascular plants probably invest in some form of toxic chemical defence that can be lethal to potential or actual herbivores. However, many insect herbivores are specialists that can handle these toxins with varying degrees of success (Bernays, 1988, 1989; Bernays & Graham, 1988) and some of the most specialized species store or sequester host plant-derived toxins and use them for their own chemical defences against natural enemies at the third trophic level (Rowell-Rahier & Pasteels, 1992). It is these sequestering specialists that pose a paradox for plants because greater investment in toxic chemical defences by a plant may lead to enhanced herbivore fitness and reduced plant fitness.

Cardenolide fingerprint of monarch butterflies reared on common milkweed,Asclepias syriaca L.

Monarch butterfly,Danaus plexippus (L.), larvae were collected during August 1983 from the common milkweed,Asclepias syriaca L., across its extensive North American range from North Dakota, east to Vermont, and south to Virginia. This confirms that the late summer distribution of breeding monarchs in eastern North America coincides with the range of this extremely abundant milkweed resource. Plant cardenolide concentrations, assayed by spectrophotometry in 158 samples from 27 collection sites, were biased towards plants with low cardenolide, and ranged from 4 to 229 μg/ 0.1 g dry weight, with a mean of 50 μg/0.1 g. Monarch larvae reared on these plants stored cardenolides logarithmically, and produced 158 adults with a normally distributed concentration range from 0 to 792 μg/0. l g dry butterfly, with a mean of 234 μg/0.1 g. Thus butterflies increased the mean plant cardenolide concentration by 4.7. The eastern plants and their resultant butterflies had higher cardenolide concentrations than those from the west, and in some areas monarchs sequestered more cardenolide from equivalent plants. Plants growing in small patches had higher cardenolide concentrations than those in larger patches, but this did not influence butterfly concentration. However, younger plants and those at habitat edges had higher cardenolide concentrations than either older, shaded, or open habitat plants, and this did influence butterfly storage. There were no apparent topographical differences reflected in the cardenolides of plants and butterflies. Twenty-eight cardenolides were recognized by thin-layer chromatography, with 27 in plants and 21 in butterflies. Butterflies stored cardenolides within the more polar 46% of the plantRd range, these being sequestered in higher relative concentrations than they occurred in the plants. By comparison with published TLC cardenolide mobilities, spots 3, 4, 9, 16, 24 or 25, 26, and 27, may be the cardenolides syrioside, uzarin, syriobioside, syriogenin, uzarigenin, labriformidin, and labriformin, respectively. Cochromatography with cardenolide standards indicated that desglucosyrioside did not occur in the plants but did occur in 70% of the butterflies, and aspecioside was in 99% of the plants and 100% of the butterflies. The polar aspecioside was the single most concentrated and diagnostic cardenolide in both plants and butterflies. ButterflyRd values were dependent on those of the plant, and both showed remarkable uniformity over the range of areas sampled. Thus contrary to previous reports,A. syriaca has a biogeographically consistent cardenolide fingerprint pattern. The ecological implications of this for understanding the monarchs annual migration cycle are significant.

Oviposition by Danaus plexippus in relation to cardenolide content of three Asclepias species in the southeastern U.S.A.

Abstract. 1. Female monarchs were observed in the field ovipositing on a native North American milkweek host, Asclepias humistrata L. As in a comparable Australian study on an introduced novel host (Asclepias fruticosa L.) we found post‐alighting rejection of plants with low and high cardiac glycoside concentration (CG).

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

SummaryCardenolide 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.

Milkweeds, monarch butterflies and the ecological significance of cardenolides

SummaryThe 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 Rothschilds 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.

Monarch Butterfly (Danaus Plexippus) Thermoregulatory Behavior and Adaptations for Overwintering in Mexico

Monarch butterflies from eastern North America migrate each fall to high altitude habitats in central Mexico and must avoid freezing, desiccation, heat stress, and predation while drawing on unrenewable lipid reserves for at least 90 d. Survival involves a heat—gaining morphology and behaviors in which thermoregulation plays a central role. Heat production by shivering permits raising of thoracic temperatures sufficiently for the butterflies to crawl up vegetation to sun—bask where they warm rapidly to flight threshold (°12.7°—16.0°C). Shivering and basking can also achieve or maintain flight temperature during partly cloudly weather. Both behaviors delay the decline of thoracic temperatures below flight threshold and consequent thermal trapping either on the ground beneath clusters of other monarchs, or while the butterflies are at water or nectar sources. The monarch thus is the first butterfly in which shivering has been shown to be of major ecological importance. At the other end of the thermal spectrum, basking in the intense insolation at this lattitude causes rapid warming at ambient temperatures as low as 9°. To avoid overheating and rapid depletion, the butterflies adopt sum—minimizing postures or fly out of insolated clusters and glide above the colony, losing heat to the cold ambient. Calculations suggest that a large proportion of the butterfies dies from depleting lipid stores. Maintenance of low body temperatures to conseve lipids is one of the major reasons why migrant monarchs select these high mountain forest as their overwinterin habitat.

PLANT LATEX AND FIRST-INSTAR MONARCH LARVAL GROWTH AND SURVIVAL ON THREE NORTH AMERICAN MILKWEED SPECIES

First-instar larvae of the monarch butterfly, Danaus plexippus, a milkweed specialist, generally grew faster and survived better on leaves when latex flow was reduced by partial severance of the leaf petiole. The outcome depended on milkweed species and was related to the amount of latex produced. The outcome also may be related to the amount of cardenolide produced by the plants as a potential chemical defense against herbivory. Growth was more rapid, but survival was similar on partially severed compared with intact leaves of the high-latex/low-cardenolide milkweed, Asclepias syriaca, whereas both growth and survival were unaffected on the low-latex/low-cardenolide milkweed A. incarnata. On the low-latex/low-cardenolide milkweed A. tuberosa, both growth and survival of larvae were only marginally affected. These results contrast sharply to previous results with the milkweed, A. humistrata, in Florida, which has both high latex and high cardenolide. Larval growth and survival on A. humistrata were both increased by partially severing leaf petioles. Larval growth rates among all four milkweed species on leaves with partially severed petioles were identical, suggesting that latex and possibly the included cardenolides are important in first-instar monarch larval growth, development, and survivorship.

Monarch butterfly voltinism: effects of temperature constraints at different latitudes.

Monarch butterflies have previously been thought to produce three to five generations in the warm southern latitudes of North America and one to two generations in cooler northern latitudes. This life history pattern is based solely on lower temperature constraints on reproduction and is unsupported by data. In contrast, we show that monarch breeding is distributed in space and time in relation to both lower and upper temperature constraints. Thus in the hot south (Florida) monarchs produce two generations between the arrival of overwintered migrants and the onset of lethally high early summer temperatures. This is followed by a further three generations at 16° latitude further north in Wisconsin. Our field-based observations are consistent with five years of predictions for Florida and Wisconsin using a simple model based on the day degrees available for reproduction and larval development, between experimentally determined lower and upper lethal temperatures. Such a pattern of fewer generations in warmer than cooler climates suggests that the offspring of spring migrants are also migratory to escape lethally high southern temperatures.

A conceptual framework for integrating hydrological and biological indicators into watershed management.

Development of integrated ecological indicators for assessment of the condition of altered watersheds is fundamental to sound policy and decision making in water resource management. This paper proposes a conceptual framework for developing and integrating a set of hydrological and biologic indicators that can show the modified spatial and temporal distributions of hydrological and biological conditions which result from land use/cover changes across the study watersheds by using Geographic Information Systems, remote sensing, multiple physical and biological databases, and simulation models. Effects of management practices and programs can be evaluated by comparing the temporal distributions of these indicators over a certain period. The paper further outlines steps needed to bridge the gaps between the largely physical and structural aspects of research on watershed indicators and the work on biological processes and indicators of ecosystems for integrating these indicators into watershed planning and management processes.