Effectiveness of tiger moth (Lepidoptera, Arctiidae) chemical defenses against an insectivorous bat (Eptesicus fuscus)

Summary. Adult tiger moths exhibit a wide range of palatabilities to the insectivorous big brown bat Eptesicus fuscus. Much of this variation is due to plant allelochemics ingested and sequestered from their larval food. By using a comparative approach involving 15 species from six tribes and two subfamilies of the Arctiidae we have shown that tiger moths feeding on cardiac glycoside-containing plants often contain highly effective natural feeding deterrents. Feeding on pyrrolizidine alkaloid-containing plants is also an effective deterrent to predation by bats but less so than feeding on plants rich in cardiac glycosides. Moths feeding on plants containing iridoid glycosides and/or moths likely to contain biogenic amines were the least deterrent. By manipulating the diet of several tiger moth species we were able to adjust their degree of palatability and link it to the levels of cardiac glycosides or pyrrolizidine alkaloids in their food. We argue that intense selective pressure provided by vertebrate predators including bats has driven the tiger moths to sequester more and more potent deterrents against them and to acquire a suite of morphology characteristics and behaviors that advertise their noxious taste.     

Multi-level complexity in the use of plant allelochemicals by aposematic insects

Summary As recognized by Miriam Rothschild as early as the 1960s and repeatedly emphasized in her papers, the use, misuse, or non-use of plant allelochemicals by insects is extremely variable and difficult to predict, at many levels of time, space, and biological organization. Although certain patterns that reoccur have been important in the development of ecological theory, the optimization of cost-benefit equations involving two or three trophic levels, each with large numbers of individuals, populations, and species in erratic and complex interactions, produces unexpected and fascinating scenarios. The development of rapid colorimetric and chromatographic analyses for several types of plant allelochemicals, notably certain groups of alkaloids, cardiac and cyanogenic glycosides, phenolics, terpenes, and glucosinolates, has permitted a detailed investigation of the variation and flow of these substances in natural organisms and ecosystems. The results of these analyses, in our hands mostly for pyrrolizidine alkaloids (PAs), do not suggest a straightforward classical choice by the aposematic insect to simply sequester or synthesize its defences. Rather, they reveal a confusing variety of diffuse and complex patterns that become increasingly closer to chaos as they are multiplied across structures, species, sexes, stages, sites, seasons, and selective regimes. We present a model reflecting results of analyses at this chemoecological interface. Depending upon an initial option, involving the recognition (or not) of a plant allelochemical, the herbivore will face thereafter options to ingest it (or not), and then to tolerate and absorb (or detoxify and excrete), modify (or not), passively, actively or selectively accumulate, turn over (or not), distribute (or concentrate), and use this compound in a variety of growth, defense, or reproductive functions. The herbivore can also quantitatively or qualitatively regulate the intensity or dispersion of its attack on the plant tissues, in order to modify feedback loops of selection on the plant and its chemicals which exist in most of the earlier steps, or those with its predators and parasites that occur in the later ones. Options that lead to mutualism through positive feedback loops will tend to accumulate and become rapidly fixed by natural selection. Additional variations and anomalies such as automimicry, chemical mimicry, sexual dimorphism and communication, selective sequestration and passing-up of allelochemicals, special glands and structures, and synergism effects, are among the secondary complications of this model that have occupied much thought, time, experimental labor, and polemical space in chemical ecology journals and meetings. Examination of the tendencies and results at various points in the model can be used to explain these features and to make further predictions, plan experiments, and devise activity-based bioassays and new chemical analyses. These may lead some day to new and more robust visions of the major patterns of chemical transfer at this widespread and important natural interface.     

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.