Multiple lepidopteran larvae feed successfully on plants containing glucosinolates despite the diverse array of toxic and deterrent breakdown products, such as isothiocyanates (ITCs), formed upon plant damage. While much is known about how specialist lepidopterans metabolize and tolerate glucosinolates, there is little information about the metabolic fate of these plant defense compounds in specialized herbivores. Employing 13C- and 14C-labeled 4-methylsulfinylbutyl glucosinolate (glucoraphanin), we identified and quantified the major detoxification products of glucosinolates and ITCs in selected specialized and generalist larvae. While specialists prevented glucosinolate hydrolysis or diverted hydrolysis to form nitriles, hydrolysis in generalists proceeded to toxic ITCs, of which a portion were conjugated to glutathione. However, a large amount of ITCs remained unmodified, which may have led to the observed negative effects on growth and development. The performance of two generalist-feeding caterpillars, Spodoptera littoralis (African cotton leafworm) and Mamestra brassicae (cabbage moth) on Arabidopsis thaliana Col-0 and various glucosinolate-deficient mutants was investigated from hatching until pupation. We found that glucosinolates negatively affected larval growth and development, but not survival, with aliphatic glucosinolates having stronger effects than indolic glucosinolates, and the combination of the two glucosinolate types being even more detrimental to growth and development. Curiously, last instar larvae grew better on wild type than on non-glucosinolate-containing plant lines, but this could not be attributed to a change in detoxification rate or feeding behavior. Glucosinolates thus appear to be effective defenses against generalist lepidopteran herbivores at least during most stages of larval development. Nevertheless, the reversal of negative effects in the oldest instar is intriguing, and further investigation of this phenomenon may shed light on how generalists adjust their physiology to feed on diets with many different types of plant defense compounds.
Plant responses to herbivory and light competition are often in opposing directions, posing a potential conflict for plants experiencing both stresses. For sun-adapted species, growing in shade typically makes plants more constitutively susceptible to herbivores via reduced structural and chemical resistance traits. Nonetheless, the impact of light environment on induced resistance has been less well-studied, especially in field experiments that link physiological mechanisms to ecological outcomes. Accordingly, we studied induced resistance of common milkweed (Asclepias syriaca, a sun-adapted plant), and linked hormonal responses, resistance traits, and performance of specialist monarch caterpillars (Danaus plexippus) in varying light environments. In natural populations, plants growing under forest-edge shade showed reduced levels of resistance traits (lower leaf toughness, cardenolides, and trichomes) and enhanced light-capture traits (higher specific leaf area, larger leaves, and lower carbon-to-nitrogen ratio) compared to paired plants in full sun. In a field experiment repeated over two years, only milkweeds growing in full sun exhibited induced resistance to monarchs, whereas plants growing in shade were constitutively more susceptible and did not induce resistance. In a more controlled field experiment, plant hormones were higher in the sun (jasmonic acid, salicylic acid, abscisic acid, indole acidic acid) and were induced by herbivory (jasmonic acid and abscisic acid). In particular, the jasmonate burst following herbivory was halved in plants raised in shaded habitats, and this correspondingly reduced latex induction (but not cardenolide induction). Thus, we provide a mechanistic basis for the attenuation of induced plant resistance in low resource environments. Additionally, there appears to be specificity in these interactions, with light-mediated impacts on jasmonate-induction being stronger for latex exudation than cardenolides.
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