The lethal plant defense paradox remains: inducible host-plant aristolochic acids and the growth and defense of the pipevine swallowtail

Toxic plants with sequestering specialists are presented with a problem because plant derived toxins protect herbivores against natural enemies. It has been suggested that early induction of toxins and later relaxation of these defenses may help the plant resolve this problem because neonate caterpillars incur the physiological cost of dealing with toxins in early life, but are denied toxins when they are able to sequester them efficiently. In California, the pipevine swallowtail, Battus philenor L. (Lepidoptera: Papilionidae), feed exclusively on Aristolochia californica Torrey (Aristolochiaceae), an endemic vine that contains toxic alkaloids called aristolochic acids that caterpillars sequester to provide chemical defense in immature and adult stages. In a field experiment, the concentration of aristolochic acids doubled in the plant following leaf damage and returned to constitutive levels after six days. Neonate pipevine swallowtail caterpillars showed no aversion to high levels of aristolochic acid in a preference test. Caterpillars reared on leaves with supplemented aristolochic acid showed no physiological cost or increased mortality compared to caterpillars reared on un-supplemented leaves. Searching efficiency and capture rate of lacewing larvae (Chrysoperla), a common predator of first instar caterpillars, was compromised significantly after feeding on caterpillars reared on leaves with supplemented concentrations of aristolochic acid compared to caterpillars feeding on control plants. Additionally, mortality of lacewings increased when they were provided with a diet of B. philenor caterpillars reared on supplemented leaves compared to caterpillars reared on control leaves. Thus, the induction of aristolochic acids in the plant following leaf damage does not resolve the problem confronted by the plant and may confer benefits to this sequestering specialist.